Consolidation of vocabulary is associated with sleep in typically developing children, but not in children with dyslexia

Abstract

Sleep is known to play an active role in consolidating new vocabulary in adults; however, the mechanisms by which sleep promotes vocabulary consolidation in childhood are less well understood. Furthermore, there has been no investigation into whether previously reported differences in sleep architecture might account for variability in vocabulary consolidation in children with dyslexia. Twenty-three children with dyslexia and 29 age-matched typically developing peers were exposed to 16 novel spoken words. Typically developing children showed overnight improvements in novel word recall; the size of the improvement correlated positively with slow wave activity, similar to previous findings with adults. Children with dyslexia showed poorer recall of the novel words overall, but nevertheless showed overnight improvements similar to age-matched peers. However, comparisons with younger children matched on initial levels of novel word recall pointed to reduced consolidation in dyslexics after 1 week. Crucially, there were no significant correlations between overnight consolidation and sleep parameters in the dyslexic group. This suggests a reduced role of sleep in vocabulary consolidation in dyslexia, possibly as a consequence of lower levels of learning prior to sleep, and highlights how models of sleep-associated memory consolidation can be usefully informed by data from typical and atypical development.

Atypicalities in sleep and semantic consolidation in autism

“…Spindles have been targeted as key to consolidation (e.g., Antony et al, ), and one previous study, to our knowledge, reports an association between overnight improvements in novel phonological knowledge and NREM spindle parameters in school‐aged children (Smith et al, ). Such data lend a developmental perspective to the predictions of the Complementary Learning Systems account of word learning (Davis & Gaskell, ), which proposes that this process engages two neural systems: the hippocampal system required for the rapid acquisition of a new word, and a slower learning neocortical system that enables strengthening of explicit knowledge as well as integration with existing vocabulary knowledge (Davis & Gaskell, ).…”

“…Thus, sleep spindles were lower in amplitude for children with ASD, compared to the amplitude of equivalent spindles in TD children. Although traditionally examined less often than spindle density, sigma power is gaining support as a robust predictor of general cognitive ability (e.g., Hoedlmoser et al, ; Tessier et al, ) and may be key to memory consolidation in developmental populations, as evidenced from studies of vocabulary consolidation (Smith et al, ) and nonverbal declarative memory (Maski et al, ). Evidence from neurotypical adults suggests that ‘spindle power’ (i.e., the average power of individually detected spindles, as opposed to the power within the sigma (spindle) frequency band, as measured here) reflects the structural integrity of an extensive network of white matter tracts including the forceps minor, parts of the uncinate fascicle and the anterior corpus callosum, as well as subcortical regions (including tracts within and around the thalamus; Piantoni et al, ).…”

“…However, an effective model of consolidation must also be able to account for individual differences. Indeed, findings of different or reduced benefits of sleep are emerging for children with ADHD (Prehn‐Kristensen et al, ), dyslexia (Smith et al, ), Williams syndrome, Down syndrome (Ashworth, Hill, Karmiloff‐Smith, & Dimitriou, ; Spanò, Gómez, Demara, Cowen, & Edgin, ) and autism spectrum disorder (ASD; Maski et al, ). Studies of neurodevelopmental disorders have the potential, therefore, to offer valuable theoretical insight into individual differences in consolidation processes (see Smith & Henderson, , for discussion of this in the context of dyslexia).…”

“…Sleep spindles have been shown to occur more frequently after learning, and have been associated with synaptic plasticity and improved retention (Muller et al, ; Rosanova & Ulrich, ). Within the domain of word learning, it has been demonstrated that overnight improvements in lexical stabilization and integration are associated with spindle characteristics measured via polysomnography in adults (Tamminen, Payne, Stickgold, Wamsley, & Gaskell, ; Weighall, Henderson, Barr, Cairney, & Gaskell, ) and children (Smith et al, ). Sleep spindle density has also been linked to the integration of new knowledge into a previously learned memory schema, and with increasing independence from hippocampus during recall the subsequent day (Hennies, Ralph, Kempkes, Cousins, & Lewis, ).…”

No effect of targeted memory reactivation during sleep on retention of vocabulary in adolescents

“…While these children show a similar overnight improvement when compared to healthy controls, slow wave and spindle power was significantly associated with overnight improvement only in healthy controls but not in dyslexic children. These findings led authors to speculate that weaker memory traces formed during encoding results in a more passive role of sleep in long-term memory consolidation 32 . Accordingly, a low performance level at learning in our sample might coincide with less stable memory traces, which in turn prevents access to sleep-dependent processes of memory consolidation (see also the discussion on the role of memory strength in sleep-dependent memory consolidation in 42 ).…”