Spatial patterns of neuronal activity in rat cerebral cortex during non-rapid eye movement sleep.

Tim Wanger,Jürgen Goldschmidt,Wolfram Wetzel,Henning Scheich,Frank W Ohl

doi:10.1007/s00429-014-0867-9

Abstract

It is commonly assumed that cortical activity in non-rapid eye movement sleep (NREMS) is spatially homogeneous on the mesoscopic scale. This is partly due to the limited observational scope of common metabolic or imaging methods in sleep. We used the recently developed technique of thallium-autometallography (TlAMG) to visualize mesoscopic patterns of activity in the sleeping cortex with single-cell resolution. We intravenously injected rats with the lipophilic chelate complex thallium diethyldithiocarbamate (TlDDC) during spontaneously occurring periods of NREMS and mapped the patterns of neuronal uptake of the potassium (K+) probe thallium (Tl+). Using this method, we show that cortical activity patterns are not spatially homogeneous during discrete 5-min episodes of NREMS in unrestrained rats—rather, they are complex and spatially diverse. Along with a relative predominance of infragranular layer activation, we find pronounced differences in metabolic activity of neighboring neuronal assemblies, an observation which lends support to the emerging paradigm that sleep is a distributed process with regulation on the local scale.Electronic supplementary materialThe online version of this article (doi:10.1007/s00429-014-0867-9) contains supplementary material, which is available to authorized users.

Highlights

Sleep is an almost ubiquitous phenomenon in the animal kingdom and is defined as a homeostatically regulated state of immobility, reduced arousal and rapid reversibility (Siegel 2005; Cirelli and Tononi 2008)
We show that cortical activity patterns are not spatially homogeneous during discrete 5-min episodes of non-rapid eye movement sleep (NREMS) in unrestrained rats—rather, F
While human positron emission tomography (PET)-studies of brain perfusion concordantly report decreases in regional cerebral blood flow throughout the cortex (Braun et al 1997; Hofle et al 1997; Maquet et al 1997; Andersson et al 1998; Kajimura et al 1999), Nofzinger et al (2002) observed relative increases in regional glucose consumption in various structures, including primary sensorimotor cortex and associational cortices

Summary

Introduction

Sleep is an almost ubiquitous phenomenon in the animal kingdom and is defined as a homeostatically regulated state of immobility, reduced arousal and rapid reversibility (Siegel 2005; Cirelli and Tononi 2008). Episodes of non-rapid eye movement sleep (NREMS) have been proposed to be critically involved in cortical plasticity processes, i.e. in the functional reorganization and/or maintenance of neuronal connections (Sejnowski and Destexhe 2000; Steriade and Timofeev 2003; Tononi and Cirelli 2006; Wang et al 2011; Chauvette et al 2012). Steriade and McCarley 2005; Buzsaki 2006), the spatial organization of cortical activity during NREMS and, in particular, to which degree it differs from wakefulness (WK) remains largely unexplored. This shortcoming is, for the most part, due to methodological difficulties. IEG expression is not suited to map activity under constant, non-stimulus conditions, where no changes in external or internal input are provided (Kovacs 2008), which makes it difficult to investigate spontaneous activity patterns during continuous NREMS episodes with this technique

Methods

Results

Conclusion