The effects of 1 week of REM sleep deprivation on parvalbumin and calbindin immunoreactive neurons in central visual pathways of kittens

Abstract

Many maturational processes in the brain are at high levels prenatally as well as neonatally before eye‐opening, when extrinsic sensory stimulation is limited. During these periods of rapid brain development, a large percentage of time is spent in rapid eye movement (REM) sleep, a state characterized by high levels of endogenously produced brain activity. The abundance of REM sleep in early life and its ensuing decline to lower levels in adulthood strongly suggest that REM sleep constitutes an integral part of the activity‐dependent processes that enable normal physiological and structural brain development. We examined the effect of REM sleep deprivation during the critical period for visual development on the development of two calcium‐binding proteins that are associated with developmental synaptic plasticity and are found in the lateral geniculate nucleus (LGN) and visual cortex. In this study, REM sleep deprivation was carried out utilizing a computer‐controlled, cage‐shaking apparatus that successfully suppressed REM sleep. Body weight data suggested that this method of REM sleep deprivation produced less stress than the classical multiple‐platform‐over‐water method. In REM sleep‐deprived animals with normal binocular vision, the number of parvalbumin‐immunoreactive (PV) neurons in LGN was found to be lower compared with control animals but was not affected in visual cortex. The pattern of calbindin‐immunoreactivity (CaB) was unchanged at either site after REM sleep deprivation. Parvalbumin‐immunoreactivity develops later than calbindin‐immunoreactivity in the LGN, and the REM sleep deprivation that we applied from postnatal day 42–49 delayed this essential step in the development of the kitten’s visual system. These data suggest that in early postnatal brain development, REM sleep facilitates the usual time course of the expression of PV‐immunoreactivity in LGN neurons.

A role for sleep in brain plasticity

“…These studies suggest that at least some effects of REM sleep deprivation on LGN cell size are mediated by the phasic processes of REM sleep. Another interesting result showed that REM sleep deprivation for 1 week decreased immunoreactivity for the calcium binding protein parvalbumin, which has been demonstrated to influence certain forms of neuronal synaptic plasticity [50], in GABAergic inter-neurons of the developing LGN [51]. Therefore, all these studies indicate that REM sleep may influence plasticity in the LGN during critical periods of visual system development [52].…”

The development of potentially better practices to support the neurodevelopment of infants in the NICU

“…This is an evidence that REM sleep facilitates the development of neuronal receptors that are associated with synaptic plasticity. 126 Additional evidence of the role of both NREM and REM sleep on ocular dominance plasticity was demonstrated in a series of four-kitten experiments. 127 This experiment used a shaking cage technique for generalized sleep deprivation.…”

Selective Rapid Eye Movement Sleep Deprivation Affects Cell Size and Number in Kitten Locus Coeruleus

“…The surgical procedure was carried out according to previously published protocols described here briefly (Oksenberg et al, 1996; Shaffery et al, 1998; Hogan et al, 2001). Animals were anesthetized with pentobarbital (40 mg/kg i.p.)…”

“…Our computer-controlled system for detection as well as deprivation of REMS was modified from a previously reported technique (Shaffery et al, 1990; Hogan et al, 2001). The system reliably identifies REMS on the basis of individually determined, minimum-amplitude threshold criteria configured from each kitten’s digitized ECoG and EMG recordings.…”