Stuart M. Fogel

The function of the sleep spindle: a physiological index of intelligence and a mechanism for sleep-dependent memory consolidation.

Until recently, the electrophysiological mechanisms involved in strengthening new memories into a more permanent form during sleep have been largely unknown. The sleep spindle is an event in the electroencephalogram (EEG) characterizing Stage 2 sleep. Sleep spindles may reflect, at the electrophysiological level, an ideal mechanism for inducing long-term synaptic changes in the neocortex. Recent evidence suggests the spindle is highly correlated with tests of intellectual ability (e.g.; IQ tests) and may serve as a physiological index of intelligence. Further, spindles increase in number and duration in sleep following new learning and are correlated with performance improvements. Spindle density and sigma (14-16Hz) spectral power have been found to be positively correlated with performance following a daytime nap, and animal studies suggest the spindle is involved in a hippocampal-neocortical dialogue necessary for memory consolidation. The findings reviewed here collectively provide a compelling body of evidence that the function of the sleep spindle is related to intellectual ability and memory consolidation.

Learning-dependent changes in sleep spindles and Stage 2 sleep

It has become increasingly clear that sleep is necessary for efficient memory consolidation. Recently, it has been found that Stage 2 sleep disruption impairs procedural memory performance, and that memory performance is correlated with the duration of Stage 2 sleep; but the mechanisms involved in synaptic plasticity for procedural memory during sleep have not been identified. The present study examined the learning‐dependent changes in sleep, including Stage 2 sleep spindles. Following an intense period of simple motor procedural learning, the duration of Stage 2 sleep and spindle density increased. There were no changes observed in the duration of any other stage of sleep or in the density of rapid eye movements. These findings support the hypothesis that sleep spindles are involved in the off‐line reprocessing of simple motor procedural memory during Stage 2 sleep.

Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems

Sleep spindles and rapid eye movements have been found to increase following an intense period of learning on a combination of procedural memory tasks. It is not clear whether these changes are task specific, or the result of learning in general. The current study investigated changes in spindles, rapid eye movements, K-complexes and EEG spectral power following learning in good sleepers randomly assigned to one of four learning conditions: Pursuit Rotor (n=9), Mirror Tracing (n=9), Paired Associates (n=9), and non-learning controls (n=9). Following Pursuit Rotor learning, there was an increase in the duration of Stage 2 sleep, spindle density (number of spindles/min), average spindle duration, and an increase in low frequency sigma power (12-14Hz) at occipital regions during SWS and at frontal regions during Stage 2 sleep in the second half of the night. These findings are consistent with previous findings that Pursuit Rotor learning is consolidated during Stage 2 sleep, and provide additional data to suggest that spindles across all non-REM stages may be a mechanism for brain plasticity. Following Paired Associates learning, theta power increased significantly at central regions during REM sleep. This study provides the first evidence that REM sleep theta activity is involved in declarative memory consolidation. Together, these findings support the hypothesis that brain plasticity during sleep does not involve a unitary process; that is, different types of learning have unique sleep-related memory consolidation mechanisms that act in dissociable brain regions at different times throughout the night.

Preserved spatial memory after hippocampal lesions: effects of extensive experience in a complex environment

Damage to the hippocampus typically impairs spatial learning and memory in animals, but humans with hippocampal lesions retain spatial memories of premorbidly familiar environments. We showed that, like humans, normal rats reared in a complex environment and then given hippocampal lesions retained allocentric spatial memory for that environment. These results, which ruled out dependency on single cues, landmarks or specific routes, suggest that extensive premorbid experience leads to spatial representations that are independent of the hippocampus.

Sleep spindles and learning potential.

The number of sleep spindles remains relatively stable within individuals from night to night. However, there is little explanation for the large interindividual differences in spindles. The authors investigated the relationship between spindles and intelligence quotient (IQ) in 3 separate studies. The number of spindles and sigma power were positively correlated with performance IQ (PIQ), but not verbal IQ (VIQ). The perceptual/analytical skills measured by the PIQ Picture Completion subscale accounted for most of the interindividual differences in spindles. Furthermore, there was a relationship between the rapid eye movements (REMs) of REM sleep and VIQ in individuals with higher IQ scores. A similar pattern was observed between spindles and PIQ. It was hypothesized that high-IQ individuals have more spindles that can support more complex cortical networks underlying perceptual/analytical abilities.

Neural correlates of the age-related changes in motor sequence learning and motor adaptation in older adults.

As the worlds population ages, a deeper understanding of the relationship between aging and motor learning will become increasingly relevant in basic research and applied settings. In this context, this review aims to address the effects of age on motor sequence learning (MSL) and motor adaptation (MA) with respect to behavioral, neurological, and neuroimaging findings. Previous behavioral research investigating the influence of aging on motor learning has consistently reported the following results. First, the initial acquisition of motor sequences is not altered, except under conditions of increased task complexity. Second, older adults demonstrate deficits in motor sequence memory consolidation. And, third, although older adults demonstrate deficits during the exposure phase of MA paradigms, the aftereffects following removal of the sensorimotor perturbation are similar to young adults, suggesting that the adaptive ability of older adults is relatively intact. This paper will review the potential neural underpinnings of these behavioral results, with a particular emphasis on the influence of age-related dysfunctions in the cortico-striatal system on motor learning.

Habitual napping moderates motor performance improvements following a short daytime nap

The effect of napping on motor performance was examined in habitual and non-habitual nappers who were randomly assigned to a nap or reading condition. Motor procedural learning and auditory discrimination tasks were administered pre- and post-condition. Both groups reported improved alertness post-nap, but not post-reading. Non-habitual nappers fell asleep faster and tended to have greater sleep efficiency, but did not differ from habitual nappers on other sleep architecture variables. Habitual nappers had greater alpha and theta EEG power in stage 1, and greater delta, alpha and sigma power in stage 2 sleep. Motor performance deteriorated for non-habitual nappers who napped, but improved for all others. The number of sleep spindles and sigma power (13.5-15 Hz) significantly predicted motor performance following the nap, for habitual nappers only. Results indicate that motor learning was consolidated in a brief nap and was associated with stage 2 spindles, but only for those who habitually take naps.

Changes in context-specificity during memory reconsolidation: Selective effects of hippocampal lesions

After acquisition, memories associated with contextual fear conditioning pass through a labile phase, in which they are vulnerable to hippocampal lesions, to a more stable state, via consolidation, in which they engage extrahippocampal structures and are resistant to such disruption. The process is accompanied by changes in the form of the memory from being context-specific to context-general. However, when revived by a reminder, stable memories once again become labile and susceptible to hippocampal disruption, and memory reconsolidation is needed to stabilize them. This study addressed two questions with respect to this reconsolidation phenomenon: (1) How do reminders reinstate a hippocampally dependent memory trace? (2) As the memory changes from a stable to a labile state after a reminder, does its form remain invariant, or does it also change? Using contextual manipulations at retrieval in a test of contextual fear conditioning, we showed that when the fear-conditioning environment served as a reminder, the reinstated memory regained its context specificity and, as a result, became vulnerable again to the effects of hippocampal lesions. By comparison, exposure to a different environment during the reminder session reinstated a version of the original memory that was dependent primarily on general features of the original context and, consequently, was less affected by hippocampal lesions. These findings, which relate loss of reactivated memories after hippocampal destruction (or inactivation) to changes in memory representation, are interpreted as consistent with the transformation hypothesis of memory processing.

Daytime sleep enhances consolidation of the spatial but not motoric representation of motor sequence memory.

Motor sequence learning is known to rely on more than a single process. As the skill develops with practice, two different representations of the sequence are formed: a goal representation built under spatial allocentric coordinates and a movement representation mediated through egocentric motor coordinates. This study aimed to explore the influence of daytime sleep (nap) on consolidation of these two representations. Through the manipulation of an explicit finger sequence learning task and a transfer protocol, we show that both allocentric (spatial) and egocentric (motor) representations of the sequence can be isolated after initial training. Our results also demonstrate that nap favors the emergence of offline gains in performance for the allocentric, but not the egocentric representation, even after accounting for fatigue effects. Furthermore, sleep-dependent gains in performance observed for the allocentric representation are correlated with spindle density during non-rapid eye movement (NREM) sleep of the post-training nap. In contrast, performance on the egocentric representation is only maintained, but not improved, regardless of the sleep/wake condition. These results suggest that motor sequence memory acquisition and consolidation involve distinct mechanisms that rely on sleep (and specifically, spindle) or simple passage of time, depending respectively on whether the sequence is performed under allocentric or egocentric coordinates.

fMRI and sleep correlates of the age-related impairment in motor memory consolidation

Behavioral studies indicate that older adults exhibit normal motor sequence learning (MSL), but paradoxically, show impaired consolidation of the new memory trace. However, the neural and physiological mechanisms underlying this impairment are entirely unknown. Here, we sought to identify, through functional magnetic resonance imaging during MSL and electroencephalographic (EEG) recordings during daytime sleep, the functional correlates and physiological characteristics of this age‐related motor memory deficit. As predicted, older subjects did not exhibit sleep‐dependent gains in performance (i.e., behavioral changes that reflect consolidation) and had reduced sleep spindles compared with young subjects. Brain imaging analyses also revealed that changes in activity across the retention interval in the putamen and related brain regions were associated with sleep spindles. This change in striatal activity was increased in young subjects, but reduced by comparison in older subjects. These findings suggest that the deficit in sleep‐dependent motor memory consolidation in elderly individuals is related to a reduction in sleep spindle oscillations and to an associated decrease of activity in the cortico‐striatal network. Hum Brain Mapp 35:3625–3645, 2014.