Abstract

Auditory learning is supported by long-term changes in the neural processing of sound. We examined these task-depend changes in auditory cortex by mapping neural sensitivity to timbre, pitch and location cues in cues in trained (n = 5), and untrained control female ferrets (n = 5). Trained animals either identified vowels in a two-alternative forced choice task (n = 3) or discriminated when a repeating vowel changed in identity or pitch (n = 2). Neural responses were recorded under anesthesia in two primary auditory cortical fields and two tonotopically organized non-primary fields. In trained animals, the overall sensitivity to sound timbre was reduced across three cortical fields compared to control animals, but maintained in a non-primary field (the posterior pseudosylvian field). While training did not increase sensitivity to timbre across auditory cortex, it did change the way in which neurons integrated spectral information with neural responses in trained animals increasing their sensitivity to first and second formant frequencies, whereas in control animals’ cortical sensitivity to spectral timbre depends mostly on the second formant. Animals trained on timbre identification were required to generalize across pitch when discriminating timbre and their neurons became less modulated by fundamental frequency relative to control animals. Finally, both trained groups showed increased spatial sensitivity and an enhanced response to sound source locations close to the midline, where the loudspeaker was located in the training chamber. These results demonstrate that training elicited widespread alterations in the cortical representation of complex sounds.

Significance Statement Learning a task can elicit widespread changes in the brain. Here, we trained animals to discriminate sound timbre using synthetic vowel sounds. Somewhat surprisingly we observed that in 3 out of 4 of the brain regions studied, neural responses became less sensitive to timbre, while in the 4th area sensitivity was maintained. This suggests that training does not simply rewire more neurons to represent learned stimuli. Neurons also changed the way in which they processed stimuli becoming more sensitive to the formant cues that determine vowel identity and tuned preferentially for the region of space in which sounds were presented during training. Together, these results suggest that learning results in complex changes in how and whether neurons represent learned sounds.