Gain neuromodulation mediates perceptual switches: evidence from pupillometry, fMRI, and RNN Modelling

Abstract

Perceptual updating has been proposed to rely upon evolving activity within a recurrent, distributed thalamocortical network whose interconnections are modulated by bursts of ascending neuromodulatory neurotransmitters, such as noradrenaline. To test this hypothesis mechanistically, we leveraged a combination of pupillometry, fMRI and recurrent neural network modelling of an ambiguous figures task. Qualitative shifts in the perceptual interpretation of an ambiguous image were associated with peaks in pupil diameter, an indirect readout of phasic bursts in neuromodulatory tone. We hypothesized that increases in neuromodulatory tone led to neural gain alteration so as to causally mediate perceptual switches. To test this hypothesis, we trained a recurrent neural network to perform an analogous perceptual categorisation task, and then manipulated the gain of the RNN to mimic the effect of neuromodulatory tone. As predicted, we observed an earlier perceptual shift as a function of heightened gain. Leveraging a low-dimensional readout of the RNN dynamics, we developed two novel predictions: perceptual switches should co-occur with peaks in low-dimensional brain state velocity and with flattened energy landscape dynamics. We used dimensionality-reduced summaries of whole-brain fMRI dynamics to independently confirm each of these predictions. These results support the role of the neuromodulatory system in the large-scale network reconfigurations that mediate abrupt changes in perception.