Learning and consolidation of novel spoken words

Abstract

Two experiments explored the neural mechanisms underlying the learning and consolidation of novel spoken words. In Experiment 1, participants learned two sets of novel words on successive days. A subsequent recognition test revealed high levels of familiarity for both sets. However, a lexical decision task showed that only novel words learned on the previous day engaged in lexical competition with similar-sounding existing words. Additionally, only novel words learned on the previous day exhibited faster repetition latencies relative to unfamiliar controls. This overnight consolidation effect was further examined using fMRI to compare neural responses to existing and novel words learned on different days prior to scanning (Experiment 2). This revealed an elevated response for novel compared with existing words in left superior temporal gyrus (STG), inferior frontal and premotor regions, and right cerebellum. Cortical activation was of equivalent magnitude for unfamiliar novel words and items learned on the day of scanning but significantly reduced for novel words learned on the previous day. In contrast, hippocampal responses were elevated for novel words that were entirely unfamiliar, and this elevated response correlated with postscanning behavioral measures of word learning. These findings are consistent with a dual-learning system account in which there is a division of labor between medial-temporal systems that are involved in initial acquisition and neocortical systems in which representations of novel spoken words are subject to overnight consolidation.

Figure 1

(A) Timeline for Experiment 1. All participants were trained on two sets of novel spoken words on successive days. On the second day, training was immediately followed by a behavioral test session comprising four behavioral tasks assessing different forms of knowledge of the newly learned words. (B) Timeline for Experiment 2. After training on two sets of novel and existing spoken words on successive days, participants were fMRI scanned and completed a behavioral test session assessing different knowledge of newly learned words. (C) Timeline of the fast sparse fMRI procedure illustrating the rapid alternation of stimulus presentation and single scan volumes. Dashed line shows an estimate of the predicted BOLD response to a single stimulus (using the canonical hemodynamic response in the SPM software), illustrating how the expected hemodynamic response is sampled over subsequent scans (cf. Orfanidou et al., 2006; Jacquemot et al., 2003).

Figure 2

(A) Lexical decision response times for real-word competitors of novel words trained on Day 1 (hence consolidated), Day 2 (unconsolidated), or untrained controls. Error bars show 1 SEM after between-subjects variability is removed, suitable for repeated measures comparisons (cf. Loftus & Masson, 1994). Statistical significance of planned pairwise comparisons (***p < .001, **p < .01, *p < .05, (*) p < .1, ns = nonsignificant). (B) Response times for novel words trained on Day 1 (consolidated), Day 2 (unconsolidated), or untrained controls in the auditory repetition test. Error bars and statistical significance as before. (C) Recognition memory performance for novel words trained on Day 1 or Day 2. (D) Rated strength of meaning for novel words trained on Day 1, Day 2, or untrained controls.

Figure 3

Brain regions showing response differences between novel and existing spoken words (pause-absent trials) in the fMRI experiment rendered onto the MNI canonical brain. (A) Untrained novel > existing words, thresholded at p < .001 uncorrected, all activations shown exceed FDR corrected p < .05. No voxels show an elevated response to existing words. (B) Unconsolidated novel > existing (comparison of items trained on Day 2) thresholded as before. (C) Consolidated novel > existing words (comparison of items trained on Day 1), thresholded at p < .001 uncorrected, no voxels approach FDR p < .05. (D) Brain regions showing an interaction between novelty and consolidation (i.e., an additional response for novel words trained on Day 2, not seen for novel words trained on Day 1), results displayed at p < .001, all peak voxels in the left hemisphere and right cerebellum exceed FDR corrected p < .05, as indicated by the arrow on the color scale. (E) Mean BOLD parameter estimate (peak of the fitted canonical HRF function on an arbitrary scale) of the peak voxel in the right cerebellum (x = 16, y = +60, z = −36) for novel and existing words in each of the training conditions. Error bars show SEM after between-subject variance has been removed, suitable for repeated measures comparisons between conditions (Loftus & Masson, 1994). (F) Response profile of a cluster of voxels in the left STG (center of mass, x = −54, y = −30, z = +6), which show an elevated response to novel words and a significant interaction between novelty and consolidation. Error bars as in panel E.

Figure 4

(A) Single slice of the MNI canonical brain showing the ROI within the left HC, defined as the portion of the AAL left HC map (white outline), which shows an additional response to pause-absent trials compared with rest thresholded at FDR p < .05 (red). (B) Response of this left HC ROI to novel words presented in the first scanning run (i.e., the first presentations for untrained items) and in later scanning runs (mean of second/third run). Error bars as in Figure 3E. Significance of statistical comparisons shown with braces as in Figure 2A. (C) Correlation between responses to untrained novel words during Session 1 in the left HC ROI and subsequent recognition memory performance for single participants. The dotted line shows the best fitting linear regression line (y = 2.66x − 1.73).