Dopamine modulates prediction error forwarding in the nonlemniscal inferior colliculus

Abstract The predictive processing framework 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 nonlemniscal inferior colliculus (IC). The drive that these feedback signals exert on the perceptual model depends on their ‘expected precision’, which determines the postsynaptic gain applied in prediction error forwarding. Expected precision is theoretically encoded by the neuromodulatory (e.g., dopaminergic) systems. To test this empirically, we recorded extracellular responses from the rat nonlemniscal IC to oddball and cascade sequences before, during and after the microiontophoretic application of dopamine or eticlopride (a D2-like receptor antagonist). Hence, we studied dopaminergic modulation on the subcortical processing of unpredictable and predictable auditory changes. Results demonstrate that dopamine reduces the net neuronal responsiveness exclusively to unexpected input, without significantly altering the processing of expected auditory events at population level. We propose that, in natural conditions, dopaminergic projections from the thalamic subparafascicular nucleus to the nonlemniscal IC could serve as a precision-weighting mechanism mediated by D2-like receptors. Thereby, the levels of dopamine release in the nonlemniscal IC could modulate the early bottom-up flow of prediction error signals in the auditory system by encoding their expected precision.