Top-down and bottom-up expectations in the prefrontal and auditory cortices

Abstract

Auditory perceptual decision-making is modulated by interactions between bottom-up (sensory-driven) and top-down (expectation-driven) processes. Despite the importance of these interactions, little is known about their underlying neural mechanisms. We investigated these mechanisms by recording neural activity in the auditory and prefrontal cortices of rhesus monkeys while they performed a challenging auditory decision-making task. The monkeys decided whether the last (“test tone”) in a sequence of tone bursts, embedded in broadband noise, was low or high frequency. Task difficulty was titrated by varying the sound level of the test tone relative to the noisy background. Bottom-up expectations were manipulated by presenting three identical low- or high-frequency tone bursts (“pre-tones”), establishing sequence regularity. Top-down processing was manipulated by presenting a visual cue that indicated the prior probability that the subsequent test-tone would be high or low frequency (“pre-cue”). The monkeys’ behavioral choices and response times were biased by both the pre-tones and the pre-cues, with stronger and more consistent effects by the pre-cues. Neural activity was modulated preferentially by the pre-tones in auditory cortex and by the pre-cues in prefrontal cortex. These findings imply functional segregation between bottom-up and top-down processing in the primate brain during auditory perceptual decision-making.