Cortical thinning and sleep slow wave activity reductions mediate age-related improvements in cognition during mid-late adolescence.

STUDY OBJECTIVES: Gains in cognitive test performance that occur during adolescence are associated with brain maturation. Cortical thinning and reduced sleep slow wave activity (SWA) are markers of such developmental changes. Here we investigate whether they mediate age-related improvements in cognition. METHODS: 109 adolescents aged 15-19 years (49 males) underwent magnetic resonance imaging, polysomnography (PSG), and a battery of cognitive tasks within a 2-month time window. Cognitive tasks assessed nonverbal intelligence, sustained attention, speed of processing and working memory and executive function. To minimize the effect of sleep history on SWA and cognitive performance, PSG and test batteries were administered only after at least 8 nights of 9-h time-in-bed (TIB) sleep opportunity. RESULTS: Age-related improvements in speed of processing (r = 0.33, p = 0.001) and nonverbal intelligence (r = 0.24, p = 0.01) domains were observed. These cognitive changes were associated with reduced cortical thickness, particularly in bilateral temporoparietal regions (rs = -0.21 to -0.45, ps < 0.05), as well as SWA (r = -0.35, p < 0.001). Serial mediation models found that ROIs in the middle/superior temporal cortices, together with SWA mediated the age-related improvement observed on cognition. CONCLUSIONS: During adolescence, age-related improvements in cognition are mediated by reductions in cortical thickness and sleep SWA.

Splitting sleep between the night and a daytime nap reduces homeostatic sleep pressure and enhances long-term memory.

Daytime naps have been linked with enhanced memory encoding and consolidation. It remains unclear how a daily napping schedule impacts learning throughout the day, and whether these effects are the same for well-rested and sleep restricted individuals. We compared memory in 112 adolescents who underwent two simulated school weeks containing 8 or 6.5 h sleep opportunities each day. Sleep episodes were nocturnal or split between nocturnal sleep and a 90-min afternoon nap, creating four experimental groups: 8 h-continuous, 8 h-split, 6.5 h-continuous and 6.5 h-split. Declarative memory was assessed with picture encoding and an educationally realistic factual knowledge task. Splitting sleep significantly enhanced afternoon picture encoding and factual knowledge under both 6.5 h and 8 h durations. Splitting sleep also significantly reduced slow-wave energy during nocturnal sleep, suggesting lower homeostatic sleep pressure during the day. There was no negative impact of the split sleep schedule on morning performance, despite a reduction in nocturnal sleep. These findings suggest that naps could be incorporated into a daily sleep schedule that provides sufficient sleep and benefits learning.

Memory performance following napping in habitual and non-habitual nappers.

STUDY OBJECTIVES: Afternoon naps benefit memory but this may depend on whether one is a habitual napper (HN; ≥1 nap/week) or non-habitual napper (NN). Here, we investigated whether a nap would benefit HN and NN differently, as well as whether HN would be more adversely affected by nap restriction compared to NN. METHODS: Forty-six participants in the nap condition (HN-nap: n = 25, NN-nap: n = 21) took a 90-min nap (14:00-15:30 pm) on experimental days while 46 participants in the Wake condition (HN-wake: n = 24, NN-wake: n = 22) remained awake in the afternoon. Memory tasks were administered after the nap to assess short-term topographical memory and long-term memory in the form of picture encoding and factual knowledge learning respectively. RESULTS: An afternoon nap boosted picture encoding and factual knowledge learning irrespective of whether one habitually napped (main effects of condition (nap/wake): ps < 0.037). However, we found a significant interaction for the hippocampal-dependent topographical memory task (p = 0.039) wherein a nap, relative to wake, benefitted habitual nappers (HN-nap vs HN-wake: p = 0.003) compared to non-habitual nappers (NN-nap vs. NN-wake: p = 0.918). Notably for this task, habitual nappers' performance significantly declined if they were not allowed to nap (HN-wake vs NN-wake: p = 0.037). CONCLUSIONS: Contrary to concerns that napping may be disadvantageous for non-habitual nappers, we found that an afternoon nap was beneficial for long-term memory tasks even if one did not habitually nap. Naps were especially beneficial for habitual nappers performing a short-term topographical memory task, as it restored the decline that would otherwise have been incurred without a nap. CLINICAL TRIAL INFORMATION: NCT04044885.

Cognitive effects of split and continuous sleep schedules in adolescents differ according to total sleep opportunity.

STUDY OBJECTIVES: We compared the basic cognitive functions of adolescents undergoing split (nocturnal sleep + daytime nap) and continuous nocturnal sleep schedules when total sleep opportunity was either below or within the recommended range (i.e. 6.5 or 8 h). METHODS: Adolescent participants (age: 15-19 year) in the 8-h split (n = 24) and continuous (n = 29) sleep groups were compared with 6.5-h split and continuous sleep groups from a previous study (n = 58). These protocols involved two baseline nights (9-h time-in-bed [TIB]), 5 nights of sleep manipulation, 2 recovery nights (9-h TIB), followed by a second cycle of sleep manipulation (3 nights) and recovery (2 nights). Cognitive performance, subjective sleepiness, and mood were evaluated daily; sleep was assessed using polysomnography. RESULTS: Splitting 6.5 h of sleep with a mid-afternoon nap offered a boost to cognitive function compared to continuous nocturnal sleep. However, when total TIB across 24 h increased to 8 h, the split and continuous sleep groups performed comparably in tests evaluating vigilance, working memory, executive function, processing speed, subjective sleepiness, and mood. CONCLUSIONS: In adolescents, the effects of split sleep on basic cognitive functions vary by the amount of total sleep obtained. As long as the total sleep opportunity across 24 h is within the recommended range, students may fulfill sleep requirements by adopting a split sleep schedule consisting of a shorter period of nocturnal sleep combined with a mid-afternoon nap, without significant impact on basic cognitive functions. CLINICAL TRIAL REGISTRATION: NCT04044885.

Reward supports flexible orienting of attention to category information and influences subsequent memory.

Preparatory control of attention facilitates the efficient processing and encoding of an expected stimulus. However, this can occur at the expense of increasing the processing cost of unexpected stimuli. Preparatory control can be influenced by motivational factors, such as the expectation of a reward. Interestingly, expectation of a high reward can increase target processing, as well as reduce the cost associated with reorienting. Using a semantic cueing paradigm, we examined the interaction of reward expectation and cue-validity on semantic judgment performance and subsequent memory. Preparatory attention was assessed with pupillometry. Valid category cueing was associated with better semantic judgment performance and better subsequent memory compared to invalidly cued items. Higher reward also resulted in a larger pre-target pupil diameter, which could be indicative of increased preparatory task engagement or arousal. Critically, higher reward also reduced reorienting cost in both semantic judgment and subsequent memory performance. Our findings suggest that reward expectation can facilitate the effective control of preparatory attention for semantic information, and can support optimal goal-directed behavior based on changing task demands.

Stimulus-response incompatibility eliminates inhibitory cueing effects with saccadic but not manual responses.

There are thought to be two forms of inhibition of return (IOR) depending on whether the oculomotor system is activated or suppressed. When saccades are allowed, output-based IOR is generated, whereas input-based IOR arises when saccades are prohibited. In a series of 4 experiments, we mixed or blocked compatible and incompatible trials with saccadic or manual responses to investigate whether cueing effects would follow the same pattern as those observed with more traditional peripheral onsets and central arrows. In all experiments, an uninformative cue was displayed, followed by a cue-back stimulus that was either red or green, indicating whether a compatible or incompatible response was required. The results showed that IOR was indeed observed for compatible responses in all tasks, whereas IOR was eliminated for incompatible trials-but only with saccadic responses. These findings indicate that the dissociation between input- and output-based forms of IOR depends on more than just oculomotor activation, providing further support for the existence of an inhibitory cueing effect that is distinct to the manual response modality.