Heterogeneous Neural Populations Research Articles

Coding of object location by heterogeneous neural populations with spatially dependent correlations in weakly electric fish.

Understanding how neural populations encode sensory stimuli remains a central problem in neuroscience. Here we performed multi-unit recordings from sensory neural populations in the electrosensory system of the weakly electric fish Apteronotus leptorhynchus in response to stimuli located at different positions along the rostro-caudal axis. Our results reveal that the spatial dependence of correlated activity along receptive fields can help mitigate the deleterious effects that these correlations would otherwise have if they were spatially independent. Moreover, using mathematical modeling, we show that experimentally observed heterogeneities in the receptive fields of neurons help optimize information transmission as to object location. Taken together, our results have important implications for understanding how sensory neurons whose receptive fields display antagonistic center-surround organization encode location. Important similarities between the electrosensory system and other sensory systems suggest that our results will be applicable elsewhere.

Two opposing hippocampus to prefrontal cortex pathways for the control of approach and avoidance behaviour

The decision to either approach or avoid a potentially threatening environment is thought to rely upon the coordinated activity of heterogeneous neural populations in the hippocampus and prefrontal cortex (PFC). However, how this circuitry is organized to flexibly promote both approach or avoidance at different times has remained elusive. Here, we show that the hippocampal projection to PFC is composed of two parallel circuits located in the superficial or deep pyramidal layers of the CA1/subiculum border. These circuits have unique upstream and downstream connectivity, and are differentially active during approach and avoidance behaviour. The superficial population is preferentially connected to widespread PFC inhibitory interneurons, and its activation promotes exploration; while the deep circuit is connected to PFC pyramidal neurons and fast spiking interneurons, and its activation promotes avoidance. Together this provides a mechanism for regulation of behaviour during approach avoidance conflict: through two specialized, parallel circuits that allow bidirectional hippocampal control of PFC.

Structure in Neural Activity during Observed and Executed Movements Is Shared at the Neural Population Level, Not in Single Neurons

In multiple cortical areas, including the motor cortex, neurons have similar firing rate statistics whether we observe or execute movements. These "congruent" neurons are hypothesized to support action understanding by participating in a neural circuit consistently activated in both observed and executed movements. We examined this hypothesis by analyzing neural population structure and dynamics between observed and executed movements. We find that observed and executed movements exhibit similar neural population covariation in a shared subspace capturing significant neural variance. Further, neural dynamics are more similar between observed and executed movements within the shared subspace than outside it. Finally, we find that this shared subspace has a heterogeneous composition of congruent and incongruent neurons. Together, these results argue that similar neural covariation and dynamics between observed and executed movements do not occur via activation of a subpopulation of congruent single neurons, but through consistent temporal activation of a heterogeneous neural population.

Coding of time-dependent stimuli in homogeneous and heterogeneous neural populations.

We compare the information transmission of a time-dependent signal by two types of uncoupled neuron populations that differ in their sources of variability: i) a homogeneous population whose units receive independent noise and ii) a deterministic heterogeneous population, where each unit exhibits a different baseline firing rate ('disorder'). Our criterion for making both sources of variability quantitatively comparable is that the interspike-interval distributions are identical for both systems. Numerical simulations using leaky integrate-and-fire neurons unveil that a non-zero amount of both noise or disorder maximizes the encoding efficiency of the homogeneous and heterogeneous system, respectively, as a particular case of suprathreshold stochastic resonance. Our findings thus illustrate that heterogeneity can render similarly profitable effects for neuronal populations as dynamic noise. The optimal noise/disorder depends on the system size and the properties of the stimulus such as its intensity or cutoff frequency. We find that weak stimuli are better encoded by a noiseless heterogeneous population, whereas for strong stimuli a homogeneous population outperforms an equivalent heterogeneous system up to a moderate noise level. Furthermore, we derive analytical expressions of the coherence function for the cases of very strong noise and of vanishing intrinsic noise or heterogeneity, which predict the existence of an optimal noise intensity. Our results show that, depending on the type of signal, noise as well as heterogeneity can enhance the encoding performance of neuronal populations.

Noise correlations in the human brain and their impact on pattern classification.

Multivariate decoding methods, such as multivoxel pattern analysis (MVPA), are highly effective at extracting information from brain imaging data. Yet, the precise nature of the information that MVPA draws upon remains controversial. Most current theories emphasize the enhanced sensitivity imparted by aggregating across voxels that have mixed and weak selectivity. However, beyond the selectivity of individual voxels, neural variability is correlated across voxels, and such noise correlations may contribute importantly to accurate decoding. Indeed, a recent computational theory proposed that noise correlations enhance multivariate decoding from heterogeneous neural populations. Here we extend this theory from the scale of neurons to functional magnetic resonance imaging (fMRI) and show that noise correlations between heterogeneous populations of voxels (i.e., voxels selective for different stimulus variables) contribute to the success of MVPA. Specifically, decoding performance is enhanced when voxels with high vs. low noise correlations (measured during rest or in the background of the task) are selected during classifier training. Conversely, voxels that are strongly selective for one class in a GLM or that receive high classification weights in MVPA tend to exhibit high noise correlations with voxels selective for the other class being discriminated against. Furthermore, we use simulations to show that this is a general property of fMRI data and that selectivity and noise correlations can have distinguishable influences on decoding. Taken together, our findings demonstrate that if there is signal in the data, the resulting above-chance classification accuracy is modulated by the magnitude of noise correlations.

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.

Efficient sensory encoding and Bayesian inference with heterogeneous neural populations.

The efficient coding hypothesis posits that sensory systems maximize information transmitted to the brain about the environment. We develop a precise and testable form of this hypothesis in the context of encoding a sensory variable with a population of noisy neurons, each characterized by a tuning curve. We parameterize the population with two continuous functions that control the density and amplitude of the tuning curves, assuming that the tuning widths vary inversely with the cell density. This parameterization allows us to solve, in closed form, for the information-maximizing allocation of tuning curves as a function of the prior probability distribution of sensory variables. For the optimal population, the cell density is proportional to the prior, such that more cells with narrower tuning are allocated to encode higher-probability stimuli and that each cell transmits an equal portion of the stimulus probability mass. We also compute the stimulus discrimination capabilities of a perceptual system that relies on this neural representation and find that the best achievable discrimination thresholds are inversely proportional to the sensory prior. We examine how the prior information that is implicitly encoded in the tuning curves of the optimal population may be used for perceptual inference and derive a novel decoder, the Bayesian population vector, that closely approximates a Bayesian least-squares estimator that has explicit access to the prior. Finally, we generalize these results to sigmoidal tuning curves, correlated neural variability, and a broader class of objective functions. These results provide a principled embedding of sensory prior information in neural populations and yield predictions that are readily testable with environmental, physiological, and perceptual data.

Quantifying the signals contained in heterogeneous neural responses and determining their relationships with task performance.

The responses of high-level neurons tend to be mixtures of many different types of signals. While this diversity is thought to allow for flexible neural processing, it presents a challenge for understanding how neural responses relate to task performance and to neural computation. To address these challenges, we have developed a new method to parse the responses of individual neurons into weighted sums of intuitive signal components. Our method computes the weights by projecting a neuron's responses onto a predefined orthonormal basis. Once determined, these weights can be combined into measures of signal modulation; however, in their raw form these signal modulation measures are biased by noise. Here we introduce and evaluate two methods for correcting this bias, and we report that an analytically derived approach produces performance that is robust and superior to a bootstrap procedure. Using neural data recorded from inferotemporal cortex and perirhinal cortex as monkeys performed a delayed-match-to-sample target search task, we demonstrate how the method can be used to quantify the amounts of task-relevant signals in heterogeneous neural populations. We also demonstrate how these intuitive quantifications of signal modulation can be related to single-neuron measures of task performance (d').

Computing with Neural Synchrony

Neurons communicate primarily with spikes, but most theories of neural computation are based on firing rates. Yet, many experimental observations suggest that the temporal coordination of spikes plays a role in sensory processing. Among potential spike-based codes, synchrony appears as a good candidate because neural firing and plasticity are sensitive to fine input correlations. However, it is unclear what role synchrony may play in neural computation, and what functional advantage it may provide. With a theoretical approach, I show that the computational interest of neural synchrony appears when neurons have heterogeneous properties. In this context, the relationship between stimuli and neural synchrony is captured by the concept of synchrony receptive field, the set of stimuli which induce synchronous responses in a group of neurons. In a heterogeneous neural population, it appears that synchrony patterns represent structure or sensory invariants in stimuli, which can then be detected by postsynaptic neurons. The required neural circuitry can spontaneously emerge with spike-timing-dependent plasticity. Using examples in different sensory modalities, I show that this allows simple neural circuits to extract relevant information from realistic sensory stimuli, for example to identify a fluctuating odor in the presence of distractors. This theory of synchrony-based computation shows that relative spike timing may indeed have computational relevance, and suggests new types of neural network models for sensory processing with appealing computational properties.

Spike sorting of heterogeneous neuron types by multimodality-weighted PCA and explicit robust variational Bayes.

This study introduces a new spike sorting method that classifies spike waveforms from multiunit recordings into spike trains of individual neurons. In particular, we develop a method to sort a spike mixture generated by a heterogeneous neural population. Such a spike sorting has a significant practical value, but was previously difficult. The method combines a feature extraction method, which we may term “multimodality-weighted principal component analysis” (mPCA), and a clustering method by variational Bayes for Student's t mixture model (SVB). The performance of the proposed method was compared with that of other conventional methods for simulated and experimental data sets. We found that the mPCA efficiently extracts highly informative features as clusters clearly separable in a relatively low-dimensional feature space. The SVB was implemented explicitly without relying on Maximum-A-Posterior (MAP) inference for the “degree of freedom” parameters. The explicit SVB is faster than the conventional SVB derived with MAP inference and works more reliably over various data sets that include spiking patterns difficult to sort. For instance, spikes of a single bursting neuron may be separated incorrectly into multiple clusters, whereas those of a sparsely firing neuron tend to be merged into clusters for other neurons. Our method showed significantly improved performance in spike sorting of these “difficult” neurons. A parallelized implementation of the proposed algorithm (EToS version 3) is available as open-source code at http://etos.sourceforge.net/.

On the interpretation of sensitivity analyses of neural responses

Responses of auditory neurons vary with many dimensions of acoustical stimuli. As a consequence, there is a difference between sensitivity to a particular dimension (e.g., ITD or level), which is assessed when only that dimension is varied while other dimensions are fixed (yielding tuning curves), and information about that dimension, which requires that all natural variability be considered. In particular, the rate of a neuron can be very sensitive to a dimension while poorly informative about it, if it is also sensitive to other dimensions. One implication is that in a multi-dimensional world, stimulus properties such as ITD are optimally coded with heterogeneous neural populations.