Neural population coding: combining insights from microscopic and mass signals

Behavior relies on the distributed and coordinated activity of neural populations. Population activity can be measured using multi-neuron recordings and neuroimaging. Neural recordings reveal how the heterogeneity, sparseness, timing, and correlation of population activity shape information processing in local networks, whereas neuroimaging shows how long-range coupling and brain states impact on local activity and perception. To obtain an integrated perspective on neural information processing we need to combine knowledge from both levels of investigation. We review recent progress of how neural recordings, neuroimaging, and computational approaches begin to elucidate how interactions between local neural population activity and large-scale dynamics shape the structure and coding capacity of local information representations, make them state-dependent, and control distributed populations that collectively shape behavior

Particle-filtering approaches for nonlinear Bayesian decoding of neuronal spike trains

The number of neurons that can be simultaneously recorded doubles every seven years. This ever increasing number of recorded neurons opens up the possibility to address new questions and extract higher dimensional stimuli from the recordings. Modeling neural spike trains as point processes, this task of extracting dynamical signals from spike trains is commonly set in the context of nonlinear filtering theory. Particle filter methods relying on importance weights are generic algorithms that solve the filtering task numerically, but exhibit a serious drawback when the problem dimensionality is high: they are known to suffer from the 'curse of dimensionality' (COD), i.e. the number of particles required for a certain performance scales exponentially with the observable dimensions. Here, we first briefly review the theory on filtering with point process observations in continuous time. Based on this theory, we investigate both analytically and numerically the reason for the COD of weighted particle filtering approaches: Similarly to particle filtering with continuous-time observations, the COD with point-process observations is due to the decay of effective number of particles, an effect that is stronger when the number of observable dimensions increases. Given the success of unweighted particle filtering approaches in overcoming the COD for continuous- time observations, we introduce an unweighted particle filter for point-process observations, the spike-based Neural Particle Filter (sNPF), and show that it exhibits a similar favorable scaling as the number of dimensions grows. Further, we derive rules for the parameters of the sNPF from a maximum likelihood approach learning. We finally employ a simple decoding task to illustrate the capabilities of the sNPF and to highlight one possible future application of our inference and learning algorithm

Neurons with stereotyped and rapid responses provide a reference frame for relative temporal coding in primate auditory cortex

The precise timing of spikes of cortical neurons relative to stimulus onset carries substantial sensory information. To access this information the sensory systems would need to maintain an internal temporal reference that reflects the precise stimulus timing. Whether and how sensory systems implement such reference frames to decode time-dependent responses, however, remains debated. Studying the encoding of naturalistic sounds in primate (Macaca mulatta) auditory cortex we here investigate potential intrinsic references for decoding temporally precise information. Within the population of recorded neurons, we found one subset responding with stereotyped fast latencies that varied little across trials or stimuli, while the remaining neurons had stimulus-modulated responses with longer and variable latencies. Computational analysis demonstrated that the neurons with stereotyped short latencies constitute an effective temporal reference for relative coding. Using the response onset of a simultaneously recorded stereotyped neuron allowed decoding most of the stimulus information carried by onset latencies and the full spike train of stimulus-modulated neurons. Computational modeling showed that few tens of such stereotyped reference neurons suffice to recover nearly all information that would be available when decoding the same responses relative to the actual stimulus onset. These findings reveal an explicit neural signature of an intrinsic reference for decoding temporal response patterns in the auditory cortex of alert animals. Furthermore, they highlight a role for apparently unselective neurons as an early saliency signal that provides a temporal reference for extracting stimulus information from other neurons

Perception of categories: from coding efficiency to reaction times

Reaction-times in perceptual tasks are the subject of many experimental and theoretical studies. With the neural decision making process as main focus, most of these works concern discrete (typically binary) choice tasks, implying the identification of the stimulus as an exemplar of a category. Here we address issues specific to the perception of categories (e.g. vowels, familiar faces, ...), making a clear distinction between identifying a category (an element of a discrete set) and estimating a continuous parameter (such as a direction). We exhibit a link between optimal Bayesian decoding and coding efficiency, the latter being measured by the mutual information between the discrete category set and the neural activity. We characterize the properties of the best estimator of the likelihood of the category, when this estimator takes its inputs from a large population of stimulus-specific coding cells. Adopting the diffusion-to-bound approach to model the decisional process, this allows to relate analytically the bias and variance of the diffusion process underlying decision making to macroscopic quantities that are behaviorally measurable. A major consequence is the existence of a quantitative link between reaction times and discrimination accuracy. The resulting analytical expression of mean reaction times during an identification task accounts for empirical facts, both qualitatively (e.g. more time is needed to identify a category from a stimulus at the boundary compared to a stimulus lying within a category), and quantitatively (working on published experimental data on phoneme identification tasks)