Neurons in sensory systems often pool inputs over arrays of presynaptic cells, giving rise to functional subunits inside a neuron’s receptive field. The organization of these subunits provides a signature of the neuron’s presynaptic functional connectivity and determines how the neuron integrates sensory stimuli. Here we introduce the method of spike-triggered non-negative matrix factorization for detecting the layout of subunits within a neuron’s receptive field. The method only requires the neuron’s spiking responses under finely structured sensory stimulation and is therefore applicable to large populations of simultaneously recorded neurons. Applied to recordings from ganglion cells in the salamander retina, the method retrieves the receptive fields of presynaptic bipolar cells, as verified by simultaneous bipolar and ganglion cell recordings. The identified subunit layouts allow improved predictions of ganglion cell responses to natural stimuli and reveal shared bipolar cell input into distinct types of ganglion cells.
Advances in neuronal recording techniques are leading to ever larger numbers of simultaneously monitored neurons. This poses the important analytical challenge of how to capture compactly all sensory information that neural population codes carry in their spatial dimension (differences in stimulus tuning across neurons at different locations), in their temporal dimension (temporal neural response variations), or in their combination (temporally coordinated neural population firing). Here we investigate the utility of tensor factorizations of population spike trains along space and time. These factorizations decompose a dataset of single-trial population spike trains into spatial firing patterns (combinations of neurons firing together), temporal firing patterns (temporal activation of these groups of neurons) and trial-dependent activation coefficients (strength of recruitment of such neural patterns on each trial). We validated various factorization methods on simulated data and on populations of ganglion cells simultaneously recorded in the salamander retina. We found that single-trial tensor space-by-time decompositions provided low-dimensional data-robust representations of spike trains that capture efficiently both their spatial and temporal information about sensory stimuli. Tensor decompositions with orthogonality constraints were the most efficient in extracting sensory information, whereas non-negative tensor decompositions worked well even on non-independent and overlapping spike patterns, and retrieved informative firing patterns expressed by the same population in response to novel stimuli. Our method showed that populations of retinal ganglion cells carried information in their spike timing on the ten-milliseconds-scale about spatial details of natural images. This information could not be recovered from the spike counts of these cells. First-spike latencies carried the majority of information provided by the whole spike train about fine-scale image features, and supplied almost as much information about coarse natural image features as firing rates. Together, these results highlight the importance of spike timing, and particularly of first-spike latencies, in retinal coding.
The brainstem plays a crucial role in sleep-wake regulation. However, the ensemble dynamics underlying sleep regulation remain poorly understood. Here, we show slow, state-predictive brainstem ensemble dynamics and state-dependent interactions between the brainstem and the hippocampus in mice. On a timescale of seconds to minutes, brainstem populations can predict pupil dilation and vigilance states and exhibit longer prediction power than hippocampal CA1 neurons. On a timescale of sub-seconds, pontine waves (P-waves) are accompanied by synchronous firing of brainstem neurons during both rapid eye movement (REM) and non-REM (NREM) sleep. Crucially, P-waves functionally interact with CA1 activity in a state-dependent manner: during NREM sleep, hippocampal sharp wave-ripples (SWRs) precede P-waves. On the other hand, P-waves during REM sleep are phase-locked with ongoing theta oscillations and are followed by burst firing of CA1 neurons. This state-dependent global coordination between the brainstem and hippocampus implicates distinct functional roles of sleep.
Estimation of mutual information between random variables has become crucial in a range of fields, from physics to neuroscience to finance. Estimating information accurately over a wide range of conditions relies on the development of flexible methods to describe statistical dependencies among variables, without imposing potentially invalid assumptions on the data. Such methods are needed in cases that lack prior knowledge of their statistical properties and that have limited sample numbers. Here we propose a powerful and generally applicable information estimator based on non-parametric copulas. This estimator, called the non-parametric copula-based estimator (NPC), is tailored to take into account detailed stochastic relationships in the data independently of the data’s marginal distributions. The NPC estimator can be used both for continuous and discrete numerical variables and thus provides a single framework for the mutual information estimation of both continuous and discrete data. By extensive validation on artificial samples drawn from various statistical distributions, we found that the NPC estimator compares well against commonly used alternatives. Unlike methods not based on copulas, it allows an estimation of information that is robust to changes of the details of the marginal distributions. Unlike parametric copula methods, it remains accurate regardless of the precise form of the interactions between the variables. In addition, the NPC estimator had accurate information estimates even at low sample numbers, in comparison to alternative estimators. The NPC estimator therefore provides a good balance between general applicability to arbitrarily shaped statistical dependencies in the data and shows accurate and robust performance when working with small sample sizes. We anticipate that the non-parametric copula information estimator will be a powerful tool in estimating mutual information between a broad range of data.
Simultaneous spike-counts of neural populations are typically modeled by a Gaussian distribution. On short time scales, however, this distribution is too restrictive to describe and analyze multivariate distributions of discrete spike-counts. We present an alternative that is based on copulas and can account for arbitrary marginal distributions, including Poisson and negative binomial distributions as well as second and higher-order interactions. We describe maximum likelihood-based procedures for fitting copula-based models to spike-count data, and we derive a so-called flashlight transformation which makes it possible to move the tail dependence of an arbitrary copula into an arbitrary orthant of the multivariate probability distribution. Mixtures of copulas that combine different dependence structures and thereby model different driving processes simultaneously are also introduced. First, we apply copula-based models to populations of integrate-and-fire neurons receiving partially correlated input and show that the best fitting copulas provide information about the functional connectivity of coupled neurons which can be extracted using the flashlight transformation. We then apply the new method to data which were recorded from macaque prefrontal cortex using a multi-tetrode array. We find that copula-based distributions with negative binomial marginals provide an appropriate stochastic model for the multivariate spike-count distributions rather than the multivariate Poisson latent variables distribution and the often used multivariate normal distribution. The dependence structure of these distributions provides evidence for common inhibitory input to all recorded stimulus encoding neurons. Finally, we show that copula-based models can be successfully used to evaluate neural codes, e.g., to characterize stimulus-dependent spike-count distributions with information measures. This demonstrates that copula-based models are not only a versatile class of models for multivariate distributions of spike-counts, but that those models can be exploited to understand functional dependencies.
2A fundamental and recurrent question in systems neuroscience is that of assessing what 3 variables are encoded by a given population of neurons. Such assessments are often 4 challenging because neurons in one brain area may encode multiple variables, and because 5 neuronal representations might be categorical (different neurons encoding different variables) or 6 mixed (individual neurons encoding a combination of variables). These issues are particularly 7 pertinent to the representation of decision variables in the orbitofrontal cortex (OFC) -an area 8 implicated in economic choices. Here we present a new algorithm to assess whether a neuronal 9 representation is categorical or mixed, and to identify the encoded variables if the 10 representation is indeed categorical. The algorithm is based on two clustering procedures, one 11 variable-independent and the other variable-based. The two partitions are then compared 12 through adjusted mutual information. The present algorithm overcomes limitations of previous 13 approaches and is widely applicable. We tested the algorithm on synthetic data and then used it 14 to examine neuronal data recorded in the primate OFC during economic decisions. Confirming 15 previous assessments, we found the neuronal representation in OFC to be categorical in nature. 16 We also found that neurons in this area encode the value of individual offers, the binary choice 17 outcome and the chosen value. In other words, during economic choice, neurons in the primate 18 OFC encode decision variables in a categorical way.3 20 Author Summary 21 Mental functions such as sensory perception or decision making ultimately rely on the activity of 22 neuronal populations in different brain regions. Much research in neuroscience is devoted to 23 understanding how different groups of neurons support specific brain functions by representing 24 behaviorally relevant variables. In this respect, one important question is whether individual 25 neurons represent single variables, or linear combination of variables. Here we developed a 26 new algorithm to assess this general issue. We then used the algorithm to examine neurons in 27 the orbitofrontal cortex (OFC) recorded while non-human primates performed economic 28 decisions. We found that different neurons represent different variables (categorical encoding). 29Specifically, neurons in the OFC encoded the value of individual offers, the binary choice 30 outcome, and the chosen value. The present results support the hypothesis that economic 31 decisions are formed within the OFC. 34A recurrent question in systems neuroscience is that of understanding what variables are 35 encoded by a given population of neurons. Addressing this issue is a prerequisite to understand 36 what role neurons play in functions such as sensation or decision making. In a typical 37 experiment, animal subjects perform some task, behavioral conditions vary along one or more 38 dimensions, and the corresponding parameter(s) define variables potentially encoded by 39 neurons i...
We develop a novel methodology for the single-trial analysis of multichannel time-varying neuroimaging signals. We introduce the space-by-time M/EEG decomposition, based on Non-negative Matrix Factorization (NMF), which describes single-trial M/EEG signals using a set of non-negative spatial and temporal components that are linearly combined with signed scalar activation coefficients. We illustrate the effectiveness of the proposed approach on an EEG dataset recorded during the performance of a visual categorization task. Our method extracts three temporal and two spatial functional components achieving a compact yet full representation of the underlying structure, which validates and summarizes succinctly results from previous studies. Furthermore, we introduce a decoding analysis that allows determining the distinct functional role of each component and relating them to experimental conditions and task parameters. In particular, we demonstrate that the presented stimulus and the task difficulty of each trial can be reliably decoded using specific combinations of components from the identified space-by-time representation. When comparing with a sliding-window linear discriminant algorithm, we show that our approach yields more robust decoding performance across participants. Overall, our findings suggest that the proposed space-by-time decomposition is a meaningful low-dimensional representation that carries the relevant information of single-trial M/EEG signals.
In recent years, our research in computational neuroscience has focused on understanding how populations of neurons encode naturalistic stimuli. In particular, we focused on how populations of neurons use the time domain to encode sensory information. In this focused review, we summarize this recent work from our laboratory. We focus in particular on the mathematical methods that we developed for the quantification of how information is encoded by populations of neurons and on how we used these methods to investigate the encoding of complex naturalistic sounds in auditory cortex. We review how these methods revealed a complementary role of low frequency oscillations and millisecond precise spike patterns in encoding complex sounds and in making these representations robust to imprecise knowledge about the timing of the external stimulus. Further, we discuss challenges in extending this work to understand how large populations of neurons encode sensory information. Overall, this previous work provides analytical tools and conceptual understanding necessary to study the principles of how neural populations reflect sensory inputs and achieve a stable representation despite many uncertainties in the environment.
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