Trial-averaged metrics, e.g. in the form of tuning curves and population response vectors, are a basic and widely accepted way of characterizing neuronal activity. But how relevant are such trial-averaged responses to neuronal computation itself? Here we present a simple test to estimate whether average responses reflect aspects of neuronal activity that contribute to neuronal processing in a specific context. The test probes two assumptions inherent in the usage of average neuronal metrics: 1. Reliability: Neuronal responses repeat consistently enough across single trial that their average response template remains recognizable to downstream regions. 2. Behavioural relevance: If a single-trial response is more similar to the average template, it will be easier for the animal to identify the correct stimulus or action. We apply this test to a large publicly available data set featuring electrophysiological recordings from 71 brain areas in behaving mice. We show that single-trial responses were less correlated to the average response template than one would expect if they represented discrete versions of the template, down-sampled to the number of spikes in the single trial. Moreover, single-trial responses were barely stimulus-specific — they could not be clearly assigned to the average response template of one stimulus. Most importantly, better-matched single-trial responses did not more accurately predict behaviour for any of the recorded brain areas. We conclude that in this data set, average responses do not seem particularly relevant to neuronal computation in a majority of brain areas, and we encourage other researchers to apply similar tests when using trial-averaged neuronal metrics.
Quantifying the amount, content and direction of communication between brain regions is key to understanding brain function. Traditional methods to analyze brain activity based on the Wiener- Granger causality principle quantify the overall information propagated by neural activity between simultaneously recorded brain regions, but do not reveal the information flow about specific features of interest (such as sensory stimuli). Here, we develop a new information theoretic measure termed Feature-specific Information Transfer (FIT), quantifying how much information about a specific feature flows between two regions. FIT merges the Wiener-Granger causality principle with information-content specificity. We first derive FIT and prove analytically its key properties. We then illustrate and test them with simulations of neural activity, demonstrating that FIT identifies, within the total information flowing between regions, the information that is transmitted about specific features. We then analyze three neural datasets obtained with different recording methods, magneto- and electro-encephalography, and spiking activity, to demonstrate the ability of FIT to uncover the content and direction of information flow between brain regions beyond what can be discerned with traditional anaytical methods. FIT can improve our understanding of how brain regions communicate by uncovering previously hidden feature-specific information flow.
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