Elsevier

Neuropsychologia

Volume 48, Issue 6, May 2010, Pages 1869-1874
Neuropsychologia

Note
ERP evidence for distinct mechanisms of fast and slow visual perceptual learning

https://doi.org/10.1016/j.neuropsychologia.2010.01.008Get rights and content

Abstract

Perceptual learning (PL) occurs not only within the first training session but also between sessions. Once acquired, the learning effects can last for a long time. By examining the time course of learning-associated ERP changes, this study explores whether fast and slow visual PL contribute to long-term preservation. Subjects first participated in a visual task for three training sessions, and were then given one test session six months later. ERP results showed that fast learning effects, as reflected by the decrement of posterior N1 and increment of posterior P2 within session 1, were preserved in session 3 but not in the test session. However, slow learning effects, as reflected by the increment of posterior N1 and decrement of frontal P170 between sessions 1 and 3, were retained completely in the test session. This study indicates that PL induces different changes in the human adult brain during and after active training, and only the delayed changes of brain activity can be preserved for a long period of six months.

Introduction

Perceptual learning (PL) represents one kind of skill learning whereby relatively permanent and consistent changes in perception take place with repeated practice or experience. PL involves consolidation of implicit memory formed by training (Squire, 2004), and its time course has drawn a great deal of attention (Alain et al., 2007, Atienza et al., 2002, Karni and Sagi, 1993, Mednick et al., 2005, Tremblay et al., 1998, Yotsumoto et al., 2008). It has been shown that a naïve subject's performance on a simple discrimination task can be significantly improved with only a few trials, a process referred to as fast learning (e.g., Poggio, Fahle, & Edelman, 1992). This fast, within-the-first-session learning is followed by relatively slow learning that accumulates across many training sessions and training days. One important finding about slow learning is that PL may even occur between sessions when no actual training is conducted (Karni & Sagi, 1993). A time period of 1 h immediately after training (Seitz et al., 2005) and various amounts of post-training sleep (Aeschbach et al., 2008, Karni et al., 1994, Matarazzo et al., 2008, Mednick et al., 2003, Stickgold et al., 2000a, Stickgold et al., 2000b) seem to be crucial for the learning to take place and to consolidate. Once acquired, the learning effect can last for a long time, from months to even years without further training (Karni and Sagi, 1993, Polat and Sagi, 1994, Polat et al., 2004, Roth et al., 2005).

From these earlier findings, an interesting question arises: whether both fast and slow learning contribute to the long-term preservation of the PL effect? Although it has been proposed that slow learning may subserve the long-term retention of some perceptual skills (Karni & Sagi, 1993), direct evidence supporting this hypothesis is lacking. Because the effects of fast and slow learning may be intermixed in behavioral measures, it is difficult to address this issue using traditional behavioral measures (i.e., psychophysical threshold, reaction time, accuracy). On the other hand, the event-related potentials (ERPs) that offer high temporal resolution with reasonable spatial resolution may provide additional information to differentiate fast and slow learning contributions to PL.

In the domain of visual research, a number of studies have used ERP and other brain imaging techniques (e.g., functional magnetic resonance imaging, fMRI) to investigate the neural mechanisms of visual PL under different time scales, from tens of minutes (Ding et al., 2003, Itier and Taylor, 2004, Scott et al., 2006, Skrandies et al., 2001, Song et al., 2005, Song et al., 2007, Wang et al., in press) to a few days (Schiltz et al., 1999, Sigman et al., 2005, Yotsumoto et al., 2008). However, to date no published study has been able to examine both the fast and slow PL-associated neural changes in the same experiment, therefore, studies directly comparing the neural mechanisms of fast and slow visual PL are still lacking. Moreover, previous studies did not provide data demonstrating the reliability of specific brain activity after training had been discontinued for months. For these reasons, it is not clear whether neural changes associated with fast or slow PL can be preserved for a long time as the changes in perceptual ability do.

In the present study, by observing the time course of learning-associated changes in different ERP components over a period of six months, we examined whether fast and slow visual PL involves differential ERP changes as well as the roles of fast and slow learning in the long-term preservation of PL. We found that fast and slow learning were reflected by different ERP changes, and only the ERP changes associated with slow learning were retained for a long period of six months. The present study provides, to our knowledge, the first electrophysiological evidence for long-term human adult brain plasticity induced by PL. A general model for perceptual and skill learning was proposed based on these findings and the literature.

Section snippets

Subjects

Ten healthy right-handed adults (21–25 years old, six male) participated in this experiment as compensated volunteers. All had normal or corrected-to-normal vision and were naïve, with no prior experience in the task. Informed consent was obtained from each subject.

Stimuli, task and procedure

A simple visual task reported in our previous studies (Ding et al., 2003, Song et al., 2005) was adopted in the present experiment. There were five stimulus patterns (Fig. 1a), each consisting of four 3.5° × 0.2° lines forming a 2 × 2

Behavioral results

Response accuracy was high (averaged 98%) and stable throughout the training and test sessions. After three consecutive training sessions, RT decreased from 558 ms in S1B1 (i.e., Block 1 in session 1) to 423 ms in S3B3 (Fig. 2a; one-way ANOVA, F(8,72) = 10.20, p = 0.001). Significant decreases in RT were observed not only between the first two blocks in session 1 (S1B1 vs S1B2: decrement 56 ± 25 ms, mean ± S.E.; t(9) = 2.28, p = 0.04), but also across two adjacent training sessions (S1B3 vs S2B1: decrement 15 ±

Discussion

The present study showed that, using RT as an index, visual skill training induced an improvement in behavioral performance not only during training, but also after training. The learning effect was largely preserved even after six months. These results are consistent with previous studies using threshold or accuracy as a measure, supporting the prevailing notion that skill learning is a multistep process continuing beyond the actual training experience (Karni and Bertini, 1997, Stickgold, 2005

Acknowledgments

This work was supported by the National Nature Science Foundation of China grants (30570605, 30600180, 30621004, 90820307), the Humanities and Social Sciences Foundation from the Ministry of Education of China (09YJAXLX025 and 09YJCXLX029), Sun Yat-Sen University 985 Projects (16000-3253187, 2006-90015-3272210), the Ministry of Science and Technology of China grants (2005CB522800), and the Knowledge Innovation Program of the Chinese Academy of Sciences. We thank Prof. Wu Li, Silu Fan, Dr. Ming

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