Neural Correlates of Context-Dependent Perceptual Enhancement in the Inferior Colliculus

Abstract

In certain situations, preceding auditory stimulation can actually result in heightened sensitivity to subsequent sounds. Many of these phenomena appear to be generated in the brain as reflections of central computations. One example is the robust perceptual enhancement (or "pop out") of a probe signal within a broadband sound whose onset time is delayed relative to the remainder of a mixture of tones. Here we show that the neural representation of such stimuli undergoes a dramatic transformation as the pathway is ascended, from an implicit and distributed peripheral code to explicitly facilitated single-neuron responses at the level of the inferior colliculus (IC) of two awake and passively listening female marmoset monkeys (Callithrix jacchus). Many key features of the IC responses directly parallel psychophysical measures of enhancement, including the dependence on the width of a spectral notch surrounding the probe, the overall level of the complex, and the duration of the preceding sound (referred to as the conditioner). Neural detection thresholds for the probe with and without the conditioner were also in qualitative agreement with analogous psychoacoustic measures. Response characteristics during the conditioners were predictive of the enhancement or suppression of the ensuing probe response: buildup responses were associated with enhancement, whereas adapting conditioner responses were more likely to result in suppression. These data can be primarily explained by a phenomenological computational model using dynamic (adapting) inhibition as a necessary ingredient in the generation of neural enhancement.