Cortical Activation Patterns Evoked by Temporally Asymmetric Sounds and Their Modulation by Learning

When complex sounds are reversed in time, the original and reversed versions are perceived differently in spectral and temporal dimensions despite their identical duration and long-term spectrum-power profiles. Spatiotemporal activation patterns evoked by temporally asymmetric sound pairs demonstrate how the temporal envelope determines the readout of the spectrum. We examined the patterns of activation evoked by a temporally asymmetric sound pair in the primary auditory field (AI) of anesthetized guinea pigs and determined how discrimination training modified these patterns. Optical imaging using a voltage-sensitive dye revealed that a forward ramped-down natural sound (F) consistently evoked much stronger responses than its time-reversed, ramped-up counterpart (revF). The spatiotemporal maximum peak (maxP) of F-evoked activation was always greater than that of revF-evoked activation, and these maxPs were significantly separated within the AI. Although discrimination training did not affect the absolute magnitude of these maxPs, the revF-to-F ratio of the activation peaks calculated at the location where hemispheres were maximally activated (i.e., F-evoked maxP) was significantly smaller in the trained group. The F-evoked activation propagated across the AI along the temporal axis to the ventroanterior belt field (VA), with the local activation peak within the VA being significantly larger in the trained than in the naïve group. These results suggest that the innate network is more responsive to natural sounds of ramped-down envelopes than their time-reversed, unnatural sounds. The VA belt field activation might play an important role in emotional learning of sounds through its connections with amygdala.