Molecular correlates of sleep and wakefulness in the brain of the white‐crowned sparrow

Abstract

In the mammalian brain, sleep and wakefulness are associated with widespread changes in gene expression. The extent to which the molecular correlates of vigilance state are conserved across phylogeny, however, is only beginning to be explored. The goal of this study was to determine whether sleep and wakefulness affect gene expression in the avian brain. To achieve this end we performed an extensive microarray analysis of gene expression during sleep, wakefulness, and short‐term sleep deprivation in the telencephalon of the white‐crowned sparrow (Zonotrichia leucophrys gambelii). We found that, as in the rodent cerebral cortex, behavioral state, independent of time of day, has widespread effects on avian brain gene expression, affecting the transcript levels of 255 genes (1.4% of all tested transcripts). Wakefulness‐related transcripts (n = 114) code for proteins involved in energy metabolism and oxidative phosphorylation, immediate early genes and transcription factors associated with activity‐dependent neural plasticity, as well as heat‐shock proteins and molecular chaperones associated with the unfolded protein response. Sleep‐related transcripts (n = 141) code for proteins involved in membrane trafficking, lipid/cholesterol synthesis, translational regulation, cellular adhesion, and cytoskeletal organization. Remarkably, despite the considerable differences in morphology and cytology between the mammalian neocortex and the avian telencephalon, the functional categories of transcripts identified in this study exhibit a significant degree of overlap with those identified in the rodent cortex.

Local sleep homeostasis in the avian brain: convergence of sleep function in mammals and birds?

“…In mammals, such plastic changes are facilitated (in part) by the potentiating and synaptogenic action of brain-derived neurotrophic factor (BDNF) expressed during wakefulness [57,60], which increases the level of SWA during subsequent sleep [61,62]. Although it is unknown whether a similar relationship exists between BDNF and SWA in birds, the expression of other genes involved in long-term potentiation is elevated during wakefulness when compared with sleep in the forebrain of whitecrowned sparrows (Zonotrichia leucophrys gambelii; [63]). …”

“…Stimulation at a frequency similar to the slow oscillation induces long-term depression [64] and so may the SWS-related burst firing of action potentials [59,65]. The neuromodulatory milieu during SWS is also conducive to depression [66] and genes involved in this process are preferentially expressed during sleep in mammals [57] and birds [63]. Regardless of the specific mechanism(s) by which SWS facilitates downscaling, several lines of evidence suggest that synapses weaken during SWS [4,7,42 -46,52,58,59].…”

Sleep Deprivation and Gene Expression

“…2, there are different methods for the sleep deprivation of animal and many ways to measure changes in gene expression profiles. Most of the studies on sleep deprivation that aim to analyze gene expression are performed in rodents (Pompeiano et al 1992(Pompeiano et al , 1997Cirelli et al 1995Cirelli et al , 2006Maloney et al 2002;Cirelli 2006;Terao et al 2006), but there are also important studies in flies , birds (Jones et al 2008), and fish (Appelbaum et al 2010). Sleep deprivation studies are often difficult to compare, due to the use of different deprivation methods, durations, and animal models.…”

“…Since sleep-dependent gene regulation produces long-term changes in behavior and physiology, it is important from a clinical point of view to understand how sleep deprivation affects health through the expression of specific genes Ledoux et al 1996;Cirelli and Tononi 2000b;Tononi and Cirelli 2001;Cirelli 2002;Terao et al 2003Terao et al , 2006Nelson et al 2004;Cirelli et al 2005;Maret et al 2007;Jones et al 2008; Thompson et al 2010;Nitabach et al 2011). Conversely, the investigation of sleep-dependent gene regulation has overarching implications for basic research on the mechanisms underlying cognition, neurogenesis, thermal balance, inflammation, metabolic turnover, and several other processes (Smith and Kelly 1988;Everson 1995;Taishi et al 2001;Guzman-Marin et al 2003, 2006Knutson et al 2007;Guess et al 2009;Mullington et al 2009;Tufik et al 2009;van Leeuwen et al 2009;Calegare et al 2010;Aldabal and Bahammam 2011;Barf et al 2012;Aydin et al 2013).…”

Salubrinal, an inhibitor of protein synthesis, promotes deep slow wave sleep

“…Sleep deprivation has also been shown to increase the expression of BiP in Drosophila (28,39), white crowned sparrow (20), mice (25,29,41), and rats (8,38,42).…”