Quantifying the information about uncertainty in neural population codes

Abstract

The activity of neural populations typically encodes more information about sensory or motor variables than can be captured by point estimates of the variables. We present and compare two approaches to quantifying this additional or ancillary information and its relationship to uncertainty: the mutual information between activity and estimation error, and the Fisher information loss, which can be interpreted in terms of curvature in information geometry. We show that deviations from Gaussianity of estimation errors, including the long tails frequently observed in human behavioural tasks, are an expected corollary of the presence of ancillary information. However, populations with similar distributions of estimation error can differ substantially in their ancillary information content depending on the noise characteristics. For a given population tuning and noise model, our results quantify an upper bound on the information about uncertainty that can be obtained from population activity alone: behaviour demonstrating knowledge in excess of this bound would indicate access to a separate source of information about uncertainty. Finally, we contrast the effects of external noise and decreasing internal signal strength on ancillary information and the Gaussianity of errors. Our work directly relates knowledge about uncertainty to non-Gaussianity in sensory estimates, and establishes a coherent theoretical foundation for investigating the basis of metacognition in neural population activity. Author summaryThe brain processes sensory evidence about the external world via inherently noisy neural activity. As a result, behavioural judgments - such as estimating the direction of a moving object - are fundamentally uncertain. While animals, including humans, routinely use uncertainty to guide decisions under risk, how neural populations represent this uncertainty remains unclear. In this work, we show how the same neural activity used to decode a sensory variable can also provide information about the estimates reliability. We introduce a mathematical framework to quantify this "ancillary information" directly from a neural populations encoding model. We demonstrate that ancillary information predicts non-Gaussianity in estimation errors and sets an upper bound on metacognitive sensitivity (how accurately subjective confidence tracks performance). Crucially, we show that neural populations with distinct noise characteristics can yield near-identical estimation errors while providing very different degrees of uncertainty information. This highlights the importance of evaluating ancillary information, not just error patterns, when comparing competing models of sensory coding.