It is unclear whether top-down processing in the auditory cortex (AC) interferes with its bottom-up analysis of sound. Recent studies indicated non-acoustic modulations of AC responses, and that attention changes a neuron's spectrotemporal tuning. As a result, the AC would seem ill-suited to represent a stable acoustic environment, which is deemed crucial for auditory perception. To assess whether top-down signals influence acoustic tuning in tasks without directed attention, we compared monkey single-unit AC responses to dynamic spectrotemporal sounds under different behavioral conditions. Recordings were mostly made from neurons located in primary fields (primary AC and area R of the AC) that were well tuned to pure tones, with short onset latencies. We demonstrated that responses in the AC were substantially modulated during an auditory detection task and that these modulations were systematically related to top-down processes. Importantly, despite these significant modulations, the spectrotemporal receptive fields of all neurons remained remarkably stable. Our results suggest multiplexed encoding of bottom-up acoustic and top-down task-related signals at single AC neurons. This mechanism preserves a stable representation of the acoustic environment despite strong non-acoustic modulations.