Dopamine gates prediction error forwarding in the cortices of the inferior colliculus

Predictive coding theory describes perception as a hierarchical predictive model of sensation. Higher-level neural structures constrain the processing at lower-level structures by suppressing synaptic activity induced by predictable sensory input. But when predictions fail, deviant input is forwarded bottom-up as prediction error to update the perceptual model. The earliest prediction error signals identified in the auditory pathway emerge from the cortices of the inferior colliculus (IC). The drive that each prediction error has on the perceptual model depends on its precision, which is theoretically encoded by the dopaminergic system. To test it empirically, we recorded single-unit responses from the rat IC cortices to oddball and cascade sequences before, during and after the microiontophoretic application of dopamine or eticlopride (a D2-like receptor antagonist). Thereby, we studied dopaminergic modulation on the subcortical processing of unpredictable and predictable auditory changes. Results demonstrate that dopamine reduces neuronal responsiveness exclusively to unexpected auditory input. High dopamine concentrations in the neuronal microdomain reduce prediction error forwarding via D2-like receptors, without significantly altering repetition suppression. Thus, already at subcortical levels of the auditory pathway, dopaminergic input to the IC gates the bottom-up flow of prediction error signals by encoding their precision.