Sex differences in endogenous cortical network activity: spontaneously recurring Up/Down states

Abstract

BackgroundSeveral molecular and cellular processes in the vertebrate brain exhibit differences between males and females, leading to sexual dimorphism in the formation of neural circuits and brain organization. While studies on large-scale brain networks provide ample evidence for both structural and functional sex differences, smaller-scale local networks have remained largely unexplored. In the current study, we investigate sexual dimorphism in cortical dynamics by means of spontaneous Up/Down states, a type of network activity that is exhibited during slow-wave sleep, quiet wakefulness, and anesthesia and is thought to represent the default activity of the cortex.MethodsUp state activity was monitored by local field potential recordings in coronal brain slices of male and female mice across three ages with distinct secretion profiles of sex hormones: (i) pre-puberty (17–21 days old), (ii) 3–9 adult (months old), and (iii) old (19–24 months old).ResultsFemale mice of all ages exhibited longer and more frequent Up states compared to aged-matched male mice. Power spectrum analysis revealed sex differences in the relative power of Up state events, with female mice showing reduced power in the delta range (1–4 Hz) and increased power in the theta range (4–8 Hz) compared to male mice. No sex differences were found in the characteristics of Up state peak voltage and latency.ConclusionsThe present study revealed for the first time sex differences in intracortical network activity, using an ex vivo paradigm of spontaneously occurring Up/Down states. We report significant sex differences in Up state properties that are already present in pre-puberty animals and are maintained through adulthood and old age.Electronic supplementary materialThe online version of this article (doi:10.1186/s13293-017-0143-9) contains supplementary material, which is available to authorized users.

Ceftriaxone modulates the acute corticosterone effects in local field potentials in the primary somatosensory cortex of anesthetized mice

“…the main finding of this study), one cannot exclude this possibility if a larger sample is analyzed. This is of particular importance since a previous report has found differences in LFPs recorded from the somatosensory cortex of male or female mice 49 . Further studies specifically comparing larger samples of male or female mice in adulthood will be required to consolidate the findings of the present exploratory study.…”

Changes in sleep EEG with aging in humans and rodents

“…Most investigations on aging were conducted with the C57BL strain [ 28 , 65 , 72 , 82 , 102 , 103 , 115 , 117 ] while a few studies investigated other strains, e.g., DBA/2J [ 28 ], the wild type from Tg2576 [ 43 ], or CBA/J [ 83 ]. Age-related changes in sleep EEG have been observed (see below), albeit they differ slightly among strains [ 28 , 41 ].…”

“…Furthermore, almost all studies except for one [ 43 ] investigated male mice. Sleep in both sexes was analyzed and compared only once by Sigalas and colleagues [ 102 ]. In general, measured sleep parameters across research groups are less consistent than in human research; thus, degree of generalization is lower.…”

“…Two of the studies investigating age-related effects on sleep EEG in mice performed their experiments in vitro using brain slices. Sigalas et al [ 102 ] analyzed the barrel cortex in slices with a thickness of 400 μm and found a shortened duration of the UP states in the old group, but no differences in either UP states’ density, slow oscillation peak amplitude, peak latency, or in the relative power of the frequencies within the delta to gamma bands. On the other hand, in stratum pyramidale of the CA1 area in hippocampal slices (450 μm thickness), Hermann et al [ 43 ] found a decline in both the sharp wave frequency and the ripple oscillation energy with age that can be explained by a loss in synaptic strength and presynaptic plasticity in the area.…”

Long-Term Effects of Early Life Seizures on Endogenous Local Network Activity of the Mouse Neocortex

“…Here we have examined the effect of chemically induced ELS on the endogenous cortical activity in brain slices from mouse cortex. Previous studies, including our own have shown that local recurrent networks formed by excitatory and inhibitory connectivity in the neocortex generate stable and self-sustaining periods of persistent activity alternating with periods of no activity, called Up and Down states, respectively – a prominent feature of the cortical activity during slow wave sleep in vivo ( Steriade et al, 1993 , 2001 ; Sanchez-Vives and McCormick, 2000 ; Cossart et al, 2003 ; MacLean et al, 2005 ; Haider et al, 2006 ; Rigas and Castro-Alamancos, 2007 , 2009 ; Poulet and Petersen, 2008 ; Rigas et al, 2015 ; Sigalas et al, 2015 , 2017 ). Such activity is maintained in cortical slice preparations, in the absence of sensory inputs or active neuromodulation, indicating that it is chiefly the outcome of intrinsic properties of local networks and hence reflects the ‘default’ activity of the cortex ( Yuste et al, 2005 ; Sanchez-Vives et al, 2017 ).…”