Spindle Activity Orchestrates Plasticity during Development and Sleep

Abstract

Spindle oscillations have been described during early brain development and in the adult brain. Besides similarities in temporal patterns and involved brain areas, neonatal spindle bursts (NSBs) and adult sleep spindles (ASSs) show differences in their occurrence, spatial distribution, and underlying mechanisms. While NSBs have been proposed to coordinate the refinement of the maturating neuronal network, ASSs are associated with the implementation of acquired information within existing networks. Along with these functional differences, separate synaptic plasticity mechanisms seem to be recruited. Here, we review the generation of spindle oscillations in the developing and adult brain and discuss possible implications of their differences for synaptic plasticity. The first part of the review is dedicated to the generation and function of ASSs with a particular focus on their role in healthy and impaired neuronal networks. The second part overviews the present knowledge of spindle activity during development and the ability of NSBs to organize immature circuits. Studies linking abnormal maturation of brain wiring with neurological and neuropsychiatric disorders highlight the importance to better elucidate neonatal plasticity rules in future research.

Can mutation‐mediated effects occurring early in development cause long‐term seizure susceptibility in genetic generalized epilepsies?

“…One broad pathogenic mechanism may be the disruption of early developmental oscillatory behavior that is critical for the refinement of neuronal networks. Discontinuous structure of EEG activity, alternating between periods of oscillatory discharges and network silence, in premature infants is thought to reflect such activity . Rodents at birth provide ideal models for investigating these early events given that they correspond to the second gestational trimester in humans .…”

“…Rodents at birth provide ideal models for investigating these early events given that they correspond to the second gestational trimester in humans . Neonatal spindle bursting is an example of an early developmental oscillatory network behavior in rodents that is similar to that seen in humans . Giant depolarizing potentials (GDPs) are localized synchronized events that can be measured in brain slices cut from rodents early in development allowing more detailed molecular mechanisms to be resolved .…”

Genetic risk factors for schizophrenia associate with sleep spindle activity in healthy adolescents

“…Sleep spindles are brief bursts of rhythmic thalamocortical oscillations in sleep electroencephalography (EEG) at the sigma frequency range of 10-16 Hz and occur mainly during stage two of non-rapid eye movement (NREM) sleep (Lüthi, 2014). They have a major role in maintenance of sleep (Cote, Epps, & Campbell, 2000 and memory consolidation during sleep (Lüthi, 2014;Ulrich, 2016), and they facilitate adaptive plasticity in synaptic connections (Clawson, Durkin, & Aton, 2016;Lindemann, Ahlbeck, Bitzenhofer, & Hanganu-Opatz, 2016).…”

Schizotypal traits are associated with sleep spindles and rapid eye movement in adolescence

“…Several studies have reported that reduced N2 sleep spindle density is associated with a higher risk of developing schizophrenia-related cognitive deficits and poor memory consolidation (Lustenberger et al, 2015;Manoach, Pan, Purcell, & Stickgold, 2016). One potential mechanism is through neural development associated with cognitive processes: greater spindle activity is thought to be a measure of brain plasticity (Lindemann, Ahlbeck, Bitzenhofer, & Hanganu-Opatz, 2016), which is likely to be impaired in neurodegenerative disorders such as schizophrenia.…”