Hold Your Methods! How Multineuronal Firing Ensembles Can Be Studied Using Classical Spike-Train Analysis Techniques

Responses of neuronal populations play an important role in the encoding of stimulus related information. However, the inherent multidimensionality required to describe population activity has imposed significant challenges and has limited the applicability of classical spike train analysis techniques. Here, we show that these limitations can be overcome. We first quantify the collective activity of neurons as multidimensional vectors (patterns). Then we characterize the behavior of these patterns by applying classical spike train analysis techniques: peri-stimulus time histograms, tuning curves and auto- and cross-correlation histograms. We find that patterns can exhibit a broad spectrum of properties, some resembling and others substantially differing from those of their component neurons. We show that in some cases pattern behavior cannot be intuitively inferred from the activity of component neurons. Importantly, silent neurons play a critical role in shaping pattern expression. By correlating pattern timing with local-field potentials, we show that the method can reveal fine temporal coordination of cortical circuits at the mesoscale. Because of its simplicity and reliance on well understood classical analysis methods the proposed approach is valuable for the study of neuronal population dynamics

Timescales of Multineuronal Activity Patterns Reflect Temporal Structure of Visual Stimuli

The investigation of distributed coding across multiple neurons in the cortex remains to this date a challenge. Our current understanding of collective encoding of information and the relevant timescales is still limited. Most results are restricted to disparate timescales, focused on either very fast, e.g., spike-synchrony, or slow timescales, e.g., firing rate. Here, we investigated systematically multineuronal activity patterns evolving on different timescales, spanning the whole range from spike-synchrony to mean firing rate. Using multi-electrode recordings from cat visual cortex, we show that cortical responses can be described as trajectories in a high-dimensional pattern space. Patterns evolve on a continuum of coexisting timescales that strongly relate to the temporal properties of stimuli. Timescales consistent with the time constants of neuronal membranes and fast synaptic transmission (5–20 ms) play a particularly salient role in encoding a large amount of stimulus-related information. Thus, to faithfully encode the properties of visual stimuli the brain engages multiple neurons into activity patterns evolving on multiple timescales