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.
Significance Statement Sound is perceived differently when it is played in the forward and reverse directions, despite that the duration and long-term spectrum profiles are identical for these time-reversed sounds. The perceptual differences must derive from the asymmetric processing of spectral transients of sounds and the temporal interactions of neuronal activity elicited by each transient. Spatiotemporal activation patterns can further our understanding of the temporally asymmetric sound processing. We for the first time imaged the distinct cortical activation evoked by a representative pair of temporally asymmetrical sounds and showed differences in the magnitude and location of the activation peaks and their latency from sound onset. Furthermore, sound recognition training enhanced neuronal activity in the belt field presumably involved in perceptual learning.
- belt Field
- Primary Auditory Field
- Sound Discrimination
- Spatiotemporal Activation
- Time-Reversed Sound
- Voltage Sensitive Dye Imaging
Authors report no conflict of interest.
Supported by Grant-in-Aid for Scientific Research (C), no. JP22500368, JP26430034, and JP15K00234 from JSPS.