Learning-induced plasticity in auditory spatial representations revealed by electrical neuroimaging

Abstract

Auditory spatial representations are likely encoded at a population level within human auditory cortices. We investigated learning-induced plasticity of spatial discrimination in healthy subjects using auditory-evoked potentials (AEPs) and electrical neuroimaging analyses. Stimuli were 100 ms white-noise bursts lateralized with varying interaural time differences. In three experiments, plasticity was induced with 40 min of discrimination training. During training, accuracy significantly improved from near-chance levels to approximately 75%. Before and after training, AEPs were recorded to stimuli presented passively with a more medial sound lateralization outnumbering a more lateral one (7:1). In experiment 1, the same lateralizations were used for training and AEP sessions. Significant AEP modulations to the different lateralizations were evident only after training, indicative of a learning-induced mismatch negativity (MMN). More precisely, this MMN at 195-250 ms after stimulus onset followed from differences in the AEP topography to each stimulus position, indicative of changes in the underlying brain network. In experiment 2, mirror-symmetric locations were used for training and AEP sessions; no training-related AEP modulations or MMN were observed. In experiment 3, the discrimination of trained plus equidistant untrained separations was tested psychophysically before and 0, 6, 24, and 48 h after training. Learning-induced plasticity lasted <6 h, did not generalize to untrained lateralizations, and was not the simple result of strengthening the representation of the trained lateralizations. Thus, learning-induced plasticity of auditory spatial discrimination relies on spatial comparisons, rather than a spatial anchor or a general comparator. Furthermore, cortical auditory representations of space are dynamic and subject to rapid reorganization.

Figure 1.

Experimental paradigm. Experiments 1 and 2 entailed three sessions, such that training, which involved active discrimination, was preceded and followed by passive listening sessions. a, b, The procedures for experiments 1 and 2 differed only in the loci of sound presentations during the pretraining (a) and post-training (b) sessions. For experiment 1, these sounds were presented to the right hemispace (i.e., the same loci as during the training session). For experiment 2, these sounds were presented to the left hemispace (i.e., the mirror-symmetric loci as during the training session). c, Experiment 3 entailed the same training session as experiments 1 and 2, as well as one pretraining and four post-training sessions (immediately after the training, 6, 24, and 48 h later). Pretraining and post-training sessions required active discrimination between pairs involving nearby positions.

Figure 2.

Behavioral results. a, Group-averaged sensitivity (d′ ± SEM) in discriminating sound lateralizations is plotted as a function of training block for experiment 1 (blue line), experiment 2 (black line), and experiment 3 (red line). Sensitivity significantly increased with training for both experiments, with no evidence of differences between participants in experiments 1, 2, and 3 (see Results for details). b, Group-averaged sensitivity (d′ ± SEM) in discriminating sound lateralizations is plotted as a function of pretraining and post-training sessions for experiment 3. The training improved discrimination performance only for pairs involving the two trained positions and did not persist over time. Exp, Experiment. *p < 0.05.

Figure 3.

Electrophysiological results comparing responses to sound lateralizations. a, Results from experiment 1 during the pretraining (left) and post-training (right) sessions. Group-averaged (n = 10) AEPs from an exemplar scalp site (frontal electrode) are plotted (voltage as a function of time). Below is an intensity plot, illustrating statistical tests across the entire electrode montage. The x-, y-, and z-axes, illustrate, respectively, time, electrode, and p value of a paired t test. The bottom-most plot within each panel displays the result of the test of global dissimilarity, which assessed topographic differences between conditions as a function of time. b, Results from experiment 2 during the pretraining (left) and post-training (right) sessions; same conventions as in a. Note that only the post-training session from experiment 1 exhibited robust response differences (see Results for details). Fz, Frontal electrode.

Figure 4.

Electrical neuroimaging results. a, The topographic pattern analyses identified seven time periods of stable topography across the collective 488 ms poststimulus period from the four conditions of experiment 1. All topographies are shown with the nasion upward and left scalp leftward. For some of these time periods, multiple topographies were identified in the group-average AEPs. These topographies are framed. The reliability of this observation at the group-average level was then assessed at the single-subject level using the fitting procedure (see Materials and Methods). b, Over the 195–250 ms poststimulus period, different maps (framed in black and dark green) described AEPs in response to the R500 and R385 conditions during the post-training but not pretraining session. There was a significant three-way interaction between session, stimulus lateralization, and map. Additional analyses further revealed a significant two-way interaction between stimulus lateralization and map. Error bars indicate SEM. c, Over the 252–299 ms poststimulus period, different maps again described AEPs in response to the R500 and R385 conditions during the post-training but not pretraining session (framed in gray and light green). As above, there was a significant three-way interaction between session, stimulus lateralization, and map. Additional analyses further revealed a significant two-way interaction between stimulus lateralization and map. Error bars indicate SEM. d, The presence of maps in response to R500 after training significantly correlates with the initial discrimination performance (d′1) (r₍₉₎ = 0.567; p < 0.05).

Figure 5.

Source estimations. Group-averaged (n = 10) LAURA distributed linear source estimations were calculated over the 195–250 ms time period pretraining and post-training and are shown in response to the R385 and R500 conditions. The mean difference between these source estimations is also shown. Both the R385 and R500 lateralizations exhibited prominent sources within the parietal cortex bilaterally. Weaker sources were also observed in the prefrontal cortex. The difference revealed weaker activations to the R500 stimulus within the left inferior parietal cortex.