Reduced neural responses to natural foreground versus background sounds in auditory cortex

In everyday hearing, listeners face the challenge of understanding behaviorally relevant foreground stimuli (speech, vocalizations) in complex backgrounds (environmental, mechanical noise). Prior studies have shown that high-order areas of human auditory cortex (AC) pre-attentively form an enhanced representation of foreground stimuli in the presence of background noise. This enhancement requires identifying and grouping the features that comprise the background so they can be removed from the foreground representation. To study the cortical computations supporting this process, we recorded single unit activity in AC of male and female ferrets during the presentation of concurrent natural sounds from these two categories. In contrast to expectations from studies in high-order AC, single-unit responses to foreground sounds were strongly reduced relative to the paired background in primary and secondary AC. The degree of reduction could not be explained by a neuron’s preference for the foreground or background stimulus in isolation but could be partially explained by spectro-temporal statistics that distinguish foreground and background categories. Responses to synthesized sounds with statistics either matched or randomized relative to natural sounds showed progressively decreased reduction of foreground responses as natural sound statistics were removed. These results challenge the expectation that cortical foreground representations emerge directly from a mixed representation in the auditory periphery. Instead, they suggest the early AC maintains a robust representation of background noise. Strong background representations may produce a distributed code, facilitating selection of foreground signals from a relatively small subpopulation of AC neurons at later processing stages. Significance statement Perception of important sounds in a world cluttered with competing background noise requires the ability to segregate relevant and irrelevant sound sources. Most prior work investigating neural mechanisms of this background/foreground contrast has supported the theory that auditory cortex activity is largely invariant to background noise, consistent with evidence from behavioral studies. However, it remains unclear what information about background noise is represented at the single-unit level. Here, contrary to prevailing theories, we show a relative dominance of single-unit responses to natural background noise over responses to natural foreground sounds in ferret auditory cortex. A robust representation of background noise in early stages of auditory cortex may be necessary for grouping features into perceptual objects and selecting information from foreground signals for preferential representation in downstream brain areas.