Deep sleep after social stress: NREM sleep slow-wave activity is enhanced in both winners and losers of a conflict

Kamphuis, Jeanine; Lancel, Marike; Koolhaas, Jaap M.; Meerlo, Peter

doi:10.1016/j.bbi.2014.12.022

Cited by 31 publications

(32 citation statements)

References 24 publications

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“…7A and B). This finding may reflect the fact that intruder and home animals were housed in the same room and that some “contagion” of the intruder effect may be evident in REMS%, known to be highly susceptible to disruption (Kamphuis et al., 2015) and promoted as empathy in recent pain literature (e.g., Langford et al., 2006, Mogil, 2015). The findings of the additional post intruder time point regarding sleep transitions are consistent with the midpoint and endpoint measures [Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies investigating the impact of social defeat on sleep architecture used paradigms that were of shorter duration ranging from a single encounter during lights off (Meerlo et al., 1997) and lights on (Kamphuis et al., 2015, Meerlo et al., 2001) to 2 consecutive days during the dark phase (Kinn Rod et al., 2014, Kinn et al., 2008). Sleep architecture analyses were followed up to 21 days post social defeat showing fragmentation of slow wave sleep (Kinn et al., 2008 c.f., however, Kinn Rod et al., 2014) and increased slow wave activity (Kamphuis et al., 2015, Meerlo et al., 1997, Meerlo et al., 2001) with significantly reduced REMS% in the early hours following defeat (Kamphuis et al., 2015).…”

Section: Discussionmentioning

confidence: 99%

“…Although stress in rats can in no way fully depict the human biobehavioral phenomenon of depression, social defeat has been useful for studying individual stress responsiveness and is cautiously acknowledged as a valid model for human depression (Chaouloff, 2013, Hollis and Kabbaj, 2014, Koolhaas et al., 2013). Biobehavioral commonalities between melancholic or endogenous depression in humans and social defeat in rats include anhedonia, operationalized as a reduced preference for sucrose water; alterations in sleep architecture or continuity; changes in weight, and hypothalamic-pituitary-adrenal (HPA) axis dysregulation (American Psychiatric Association, 2013, Becker et al., 2008, Kamphuis et al., 2015, Patki et al., 2013, Razzoli et al., 2007, Rygula et al., 2006, Stetler and Miller, 2011). The administration of an antidepressant has been shown to significantly reduce the social defeat-induced anhedonia (Becker et al., 2008, Rygula et al., 2006) and HPA axis changes (Becker et al., 2008).…”

Section: Introductionmentioning

confidence: 99%

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Sex differences in sleep, anhedonia, and HPA axis activity in a rat model of chronic social defeat

Page

Opp

Kozachik

2016

Neurobiology of Stress

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Repeated bouts of a major stressor such as social defeat are well known to induce a depression phenotype in male rats. Despite strong evidence and acknowledgement that women have a two-fold lifetime greater risk of developing major depression compared to men, the inclusion of female rats in studies employing social defeat are very rare; their absence is attributed to less aggressive interactions. This study sought to compare in male and female rats the impact of repeated social defeat, three times per week for four weeks, on the development of changes in sleep architecture and continuity, sucrose preference as a measure of anhedonia, changes in body weight, and basal plasma corticosterone levels. We found significant reductions in rapid eye movement sleep (REMS) during the light phase in both females and males, and significant increases in numbers of vigilance state transitions during the early dark phase in females but not in males. Additionally, females exhibited significantly greater reductions in sucrose intake than males. On the other hand, no sex differences in significantly elevated basal corticosterone levels were evident, and only the males exhibited changes in body weight. Taken together these findings suggest that the inclusion of female rats in studies of social defeat may offer greater insights in studies of stress and depression.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Sex differences in sleep, anhedonia, and HPA axis activity in a rat model of chronic social defeat

Page

Opp

Kozachik

2016

Neurobiology of Stress

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“…Sleep and waking states were manually scored in 10-second epochs based on the cortical EEG and nuchal EMG. Scoring performance of the automated system was evaluated by the commonly used measure of percent agreement, in which the number of a given state scored by the automated system matching that scored manually is divided by the total number of the state scored manually (Benington et al, 1994; Diba and Buzsáki, 2007; Havekes et al, 2014; Kamphuis et al, 2015; Kempler and Richmond, 2012; Meerlo et al, 2008; O'Callaghan et al, 2007; Paul et al, 2014; Prince et al, 2014; Prince and Abel, 2013; Ruigt et al, 1989; Sanford et al, 2014; Smith and MacNeill, 1994; Witting et al, 1996). In order to analyze differences in sleep architecture between manipulations, the amount of time in each state was analyzed, and percentages were compared across experimental conditions.…”

Section: Methodsmentioning

confidence: 99%

Stress-free automatic sleep deprivation using air puffs

Gross

Vanderheyden

Urpa

et al. 2015

Journal of Neuroscience Methods

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Background Sleep deprivation via gentle handling is time-consuming and personnel-intensive. New Method We present here an automated sleep deprivation system via air puffs. Implanted EMG and EEG electrodes were used to assess sleep/waking states in six male Sprague-Dawley rats. Blood samples were collected from an implanted intravenous catheter every 4 hours during the 12-hour light cycle on baseline, 8 hours of sleep deprivation via air puffs, and 8 hours of sleep deprivation by gentle handling days. Results The automated system was capable of scoring sleep and waking states as accurately as our offline version (~90% for sleep) and with sufficient speed to trigger a feedback response within an acceptable amount of time (1.76 s). Manual state scoring confirmed normal sleep on the baseline day and sleep deprivation on the two manipulation days (68% decrease in non-REM, 63% decrease in REM, and 74% increase in waking). No significant differences in levels of ACTH and corticosterone (stress hormones indicative of HPA axis activity) were found at any time point between baseline sleep and sleep deprivation via air puffs. Comparison with Existing Method There were no significant differences in ACTH or corticosterone concentrations between sleep deprivation by air puffs and gentle handling over the 8-hour period. Conclusions Our system accurately detects sleep and delivers air puffs to acutely deprive rats of sleep with sufficient temporal resolution during the critical 4-5 h post learning sleep-dependent memory consolidation period. The system is stress-free and a viable alternative to existing sleep deprivation techniques.

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“…Different stress situations affect the sleep architecture in rodents differently; restraint stress markedly enhanced REM sleep and mildly affected NREM sleep in mice [33], whereas with foot shock stress, total NREM sleep and REM sleep was reduced [34,35]. Psychological social defeat stress has been shown to promote NREM sleep in mice [33] and rats [36,37]; however, other reports show that the sleep of socially defeated rats and mice was unaffected with regards to sleep onset, total sleep time, amount of deep sleep, changes in REM sleep, and related EEG power [38,39]. Social stress may also affect the duration of specific vigilance states.…”

Section: Discussionmentioning

confidence: 99%

Simultaneous Changes in Sleep, qEEG, Physiology, Behaviour and Neurochemistry in Rats Exposed to Repeated Social Defeat Stress

Ahnaou

Drinkenburg²

2016

Neuropsychobiology

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Depression is a heterogeneous disorder characterized by alterations at psychological, behavioural, physiological, neurophysiological, and neurochemical levels. Social stress is a prevalent stress in man, and the repeated social defeat stress model in rats has been proposed as being the rodent equivalent to loss of control, which in subordinate animals produces alterations that resemble several of the cardinal symptoms found in depressed patients. Here, rats followed a resident-intruder protocol for 4 consecutive days during which behavioural, physiological, and electroencephalographic (EEG) parameters were simultaneously monitored in subordinate rats. On day 5, prefrontal dopamine (DA) and hippocampal serotonin (5-HT) as well as corticosterone were measured in submissive rats that had visual, acoustic, and olfactory (but no physical) contact with a dominant, resident conspecific rat. Socially defeated rats demonstrated increases in ultrasonic vocalizations (20-25 KHz), freezing, submissive defensive behaviour, inactivity, and haemodynamic response, while decreases were found in repetitive grooming behaviour and body weight. Additionally, alterations in the sleep-wake architecture were associated with reduced active waking, enhanced light sleep, and increased frequency of transitions from light sleep to quiet wakefulness, indicating sleep instability. Moreover, the attenuation of EEG power over the frequency range of 4.2-30 Hz, associated with a sharp transient increase in delta oscillations, appeared to reflect increased brain activity and metabolism in subordinate animals. These EEG changes were synchronous with a marked increase in body temperature and a decrease in locomotor activity. Furthermore, psychosocial stress consistently increased 5-HT, DA, and corticosterone levels.The increased levels of cortical DA and hippocampal 5-HT during social threat may reflect a coping mechanism to promote alertness and psychological adaptation to provocative and threatening stimuli. These neurophysiological changes are hypothesized to be the consequence of dynamics in monoamine systems, which could be useful markers for disease progression in the aetiology of depression.

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Deep sleep after social stress: NREM sleep slow-wave activity is enhanced in both winners and losers of a conflict

Cited by 31 publications

References 24 publications

Sex differences in sleep, anhedonia, and HPA axis activity in a rat model of chronic social defeat

Sex differences in sleep, anhedonia, and HPA axis activity in a rat model of chronic social defeat

Stress-free automatic sleep deprivation using air puffs

Simultaneous Changes in Sleep, qEEG, Physiology, Behaviour and Neurochemistry in Rats Exposed to Repeated Social Defeat Stress

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