The fingerprints of pupillary dynamics

Abstract

The size of the pupils reflects directly the balance of different branches of the autonomic nervous system. This measure is inexpensive, non-invasive, and has provided invaluable insights on a wide range of mental processes, from attention to emotion and executive functions. Two outstanding limitations of current pupillometry research are the lack of consensus in the analytical approaches, which vary wildly across research groups and disciplines, and the fact that, unlike other neuroimaging techniques, pupillometry lacks the dimensionality to shed light on the different sources of the observed effects. In other words, pupillometry provides an integrated readout of several distinct networks, but it is unclear whether each has a specific fingerprint, stemming from its function or physiological substrate. Here we show that phasic changes in pupil size are inherently low-dimensional, with modes that are highly consistent across behavioral tasks of very different nature, suggesting that these changes occur along pupillary manifolds that are highly constrained by the underlying physiological structures rather than functions. These results provide not only a unified approach to analyze pupillary data, but also the opportunity for physiology and psychology to refer to the same processes by tracing the sources of the reported changes in pupil size in the underlying biology. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=105 SRC="FIGDIR/small/595554v3_ufig1.gif" ALT="Figure 1"> View larger version (29K): org.highwire.dtl.DTLVardef@219856org.highwire.dtl.DTLVardef@1984694org.highwire.dtl.DTLVardef@41def7org.highwire.dtl.DTLVardef@953692_HPS_FORMAT_FIGEXP M_FIG C_FIG Significance statementPhasic changes in pupil size are thought to reflect dynamic shifts between attentional states as instantiated by the locus-coeruleus noradrenaline system, and are crucial for adaptive behaviors. We found that the latent space of these changes is low-dimensional and remarkably similar across very different tasks, involving distinct cognitive processes. We therefore introduce the notion of pupillary manifolds as latent spaces that subtend the generative processes behind these changes. We suggest that manifolds arise due to hard constraints in the underlying physiological substrate - the relative balance between sympathetic and parasympathetic activity. In the framework outlined here, these mechanisms can be accessed and described directly, with only a handful of parameters, thus better informing computational modelling.