Repeated stimulus exposure alters the way sound is encoded in the human brain

Abstract

Auditory training programs are being developed to remediate various types of communication disorders. Biological changes have been shown to coincide with improved perception following auditory training so there is interest in determining if these changes represent biologic markers of auditory learning. Here we examine the role of stimulus exposure and listening tasks, in the absence of training, on the modulation of evoked brain activity. Twenty adults were divided into two groups and exposed to two similar sounding speech syllables during four electrophysiological recording sessions (24 hours, one week, and up to one year later). In between each session, members of one group were asked to identify each stimulus. Both groups showed enhanced neural activity from session-to-session, in the same P2 latency range previously identified as being responsive to auditory training. The enhancement effect was most pronounced over temporal-occipital scalp regions and largest for the group who participated in the identification task. The effects were rapid and long-lasting with enhanced synchronous activity persisting months after the last auditory experience. Physiological changes did not coincide with perceptual changes so results are interpreted to mean stimulus exposure, with and without being paired with an identification task, alters the way sound is processed in the brain. The cumulative effect likely involves auditory memory; however, in the absence of training, the observed physiological changes are insufficient to result in changes in learned behavior.

Figure 1. Flowchart describing the procedure.

Figure 2. Group averaged P1-N1-P2 complexes recorded from electrode site Cz.

Regardless of stimulus type (“mba” or “ba”), P2 peak amplitudes significantly increased across three sessions for Group 2 (exposure + task) but not Group 1 (exposure only). Sessions 1 and 2 were conducted on two consecutive days. Session 3 was conducted one week later.

Figure 3. Results from Mean-Centering PLS analyses.

(A) Electrode Montage. To report PLS results, Electrode locations were classified into 11 sagittal layers indicated by the dotted lines: three lateral (lat1–3), two medial layers (med1–2) in the two hemispheres, and one midline layer (mid). (B) Contrast weights identified for the first significant LV. For each stimulus type, the largest difference was observed between Sessions 1 and 3, in the P2 latency range, for both groups, but the degree of difference was greater in Group 2. (C) Spatiotemporal patterns of electrode saliencies and bootstrap results corresponding to the design LV shown in (B). The x-axis represents time in milliseconds (ms) starting at the stimulus onset marked as 0 ms. The y-axis represents electrodes organized in 11 blocks corresponding to the 11 sagittal layers in the montage shown in (A). Within each block, electrodes are ordered from top to bottom representing anterior to posterior sites. Each horizontal color bar represents temporal patterns of the electrode saliencies for a given electrode. Warm (more red) color illustrates time points with positive differences expressed in the design contrasts; cool (more blue) color expresses those of negative. Positive saliencies (warm color), and negative saliencies (cool color) indicate time points at which the amplitude of the AEP was enhanced over three experimental sessions. Saliencies are scaled with the singular value. For each electrode, horizontal black bars (comprised of individual “x”s) are plotted over the color contrasts to identify the time points at which differences expressed in the contrasts were stable across participants (bootstrap ratios >3).

Figure 4. Results from Non-rotated PLS analyses and AEP waveforms for selected electrodes.

Saliencies are displayed as waveforms and the circles on the top or bottom of each waveform indicate time points at which bootstrap ratios were above threshold. Larger and reliable saliencies were observed in the time range of P2 responses. Topographical maps illustrate the scalp distribution of the session effect on P2 responses. Displayed are AEP differences between Sessions 1 and 3 averaged over 190–290 ms.

Figure 5. P2 amplitude changes across Sessions at three ROIs.

Increases in P2 amplitude were most prevalent within the temporal-occipital region for both Groups across sessions. This session effect was not observed at anterior-central areas as well as at vertex (Cz) for Group 1.

Figure 6. Retention Data.

Individual P2 peak amplitude data are shown for all four Sessions in response to the stimulus “mba”. Results shown are from electrode site TP9. When looking at individual subjects, enhanced P2 amplitudes can be seen for many individuals (in Group 2) even though they had not heard these sounds for many months.

Figure 7. Group d-prime scores and standard error bars are shown for each test session.