Elsevier

Cognition

Volume 128, Issue 3, September 2013, Pages 280-286
Cognition

Brief article
Sleep restores loss of generalized but not rote learning of synthetic speech

https://doi.org/10.1016/j.cognition.2013.04.007Get rights and content

Abstract

Sleep-dependent consolidation has been demonstrated for declarative and procedural memory but few theories of consolidation distinguish between rote and generalized learning, suggesting similar consolidation should occur for both. However, studies using rote and generalized learning have suggested different patterns of consolidation may occur, although different tasks have been used across studies. Here we directly compared consolidation of rote and generalized learning using a single speech identification task. Training on a large set of novel stimuli resulted in substantial generalized learning, and sleep restored performance that had degraded after 12 waking hours. Training on a small set of repeated stimuli primarily resulted in rote learning and performance also degraded after 12 waking hours but was not restored by sleep. Moreover performance was significantly worse 24-h after rote training. Our results suggest a functional dissociation between the mechanisms of consolidation for rote and generalized learning which has broad implications for memory models.

Introduction

The acquisition of complex skills depends on the ability to generalize beyond exact situations experienced during learning. It has been argued that the ability to generalize is the defining feature of adaptive learning, and the quality that distinguishes it from simple associative memory (Poggio & Bizzi, 2004). Many models of memory suggest that generalized learning relies on the same underlying associative mechanisms as learning of specific experiences; generalization depends on abstraction from associations acquired during training (e.g., Goldinger, 1998, Hintzman, 1986, McClelland and Rumelhart, 1985). In contrast, other theories suggest that memory involves both specific representations and abstract representations (cf. Anderson et al., 2004, Grossberg, 1986, Posner and Keele, 1968). Evidence suggesting that there may be different mechanisms underlying rote and generalized learning would present a challenge for models that posit only specific representations and would provide support for models that allow for both specific and abstract representations. Here we report that the two forms of learning show different patterns of sleep-dependent consolidation.

Memory consolidation research suggests that sleep consolidates procedural and perceptual skills (see Margoliash and Fenn, 2008, McGaugh, 2000, Walker, 2005, for reviews) but the vast majority of this research has emphasized tasks wherein learning is restricted to the exact information encountered during training. Tasks used to study procedural consolidation typically focus on learning one motor pattern (cf. Fischer, Hallschmid, Elsner, & Born, 2002) or discrimination of one visual pattern (cf. Karni, Tanne, Rubenstein, Askenasy, & Sagi, 1994) which may be considered rote procedural learning. In rote motor learning, sleep is reported to enhance learning; performance is significantly better after sleep than after training, an effect not seen after an equal interval of wakefulness (cf. Fischer et al., 2002, Walker et al., 2003). Although several studies have reported this effect, recent work has argued that apparent memory enhancements may be explained by reactive inhibition (Rickard, Cai, Rieth, Jones, & Ard, 2008) or circadian differences at test (Cai & Rickard, 2009).

Although some of the work in rote procedural learning has been questioned, there is strong evidence that sleep consolidates generalized learning and promotes abstraction of information. In generalized procedural learning, performance degrades across waking retention and is restored by sleep. Sleep also inoculates memory against subsequent degradation (Brawn et al., 2008, Fenn et al., 2003). Consistent with this, we have reported that after controlling for reactive inhibition, rote motor learning follows the same general pattern of waking degradation and restoration after sleep (Brawn, Fenn, Nusbaum, & Margoliash, 2010). Other studies that have investigated generalized learning and sleep have shown that sleep can restructure information acquired during waking. Of note, Wagner, Gais, Haider, Verleger, and Born (2004) trained participants on a complex algorithm that contained a hidden rule that allowed the problem to be solved in fewer steps. Participants were more likely to become aware of the hidden rule if tested after sleep than after a waking interval. Similarly, infants who were exposed to an artificial language showed evidence of generalization and abstraction of the rules of the language after a nap. In contrast, after a waking interval, infants showed stronger veridical memory, but did not show any evidence of abstraction or generalization (Gomez, Bootzin, & Nadel, 2006). Thus, there is strong evidence that sleep consolidates generalized learning and promotes abstraction or restructuring of information.

Given that sleep consolidates both rote and generalized learning, the potential difference in consolidation of these types of learning can be used to investigate whether different mechanisms underlie these two forms of learning. Consolidation in rote skills may be confined to lower-level cortices (cf. Karni & Bertini, 1997) whereas generalized learning may depend on the interaction of broader networks of neural activity (Ahissar & Hochstein, 2004; Poggio & Bizzi, 2004). Generalized skills may receive a different benefit from consolidation processes and may be more susceptible to waking interference.

The effects of sleep on rote and generalized learning have only been compared across substantially different tasks, complicating interpretation of differences. We compared rote and generalized learning in a synthetic speech learning task and tested the effect of waking retention and sleep on performance.

Section snippets

Participants

We recruited 67 right-handed native English speakers who had no history of speech, hearing, or memory disorders. Nine participants were excluded from all analyses for not being native English speakers (n = 4), or for consuming alcohol on the study evening (n = 1), or for not completing the experiment (n = 4). The remaining 58 participants (32 female) had a mean age of 20.6 ± 3.6 (s.d.) years. All were students or employees at the University of Chicago and were financially compensated.

Materials

Seven hundred

Results

To assess immediate, practice-dependent improvements, we compared Pretest and Posttest I performance for novel and repeated words for the experimental groups. Performance was calculated as percent correct identification. Stimulus identification was scored as correct if the correct phonetic content of the word was identified. Incorrect spelling was not penalized (e.g. the word “kar” was scored correct if the stimulus was “car”). We first assessed performance on novel words by comparing

Discussion

The present study demonstrates one fundamental difference between rote and generalized learning. Sleep consolidated generalized learning but by comparison, rote memorization of 20 specific patterns did not evince any benefit from sleep-related consolidation processes. Following generalization training, recognition performance significantly degraded across waking and was restored after sleep. After rote training, performance diminished over waking retention, was not restored by sleep, and was

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