An Adolescent Sensitive Period for Social Dominance Hierarchy Plasticity Is Regulated by Cortical Plasticity Modulators in Mice

Social dominance hierarchies are a common adaptation to group living and exist across a broad range of the animal kingdom. Social dominance is known to rely on the prefrontal cortex (PFC), a brain region that shows a protracted developmental trajectory in mice. However, it is unknown to what extent the social dominance hierarchy is plastic across postnatal development and how it is regulated. Here we identified a sensitive period for experience-dependent social dominance plasticity in adolescent male mice, which is regulated by mechanisms that affect cortical plasticity. We show that social dominance hierarchies in male mice are already formed at weaning and are highly stable into adulthood. However, one experience of forced losing significantly reduces social dominance during the adolescent period but not in adulthood, suggesting adolescence as a sensitive period for experience-dependent social dominance plasticity. Notably, robust adolescent plasticity can be prolonged into adulthood by genetic deletion of Lynx1, a molecular brake that normally limits cortical plasticity through modulation of cortical nicotinic signaling. This plasticity is associated with increased activation of established nodes of the social dominance network including dorsal medial PFC and medial dorsal thalamus evidenced by increased c-Fos. Pharmacologically mediated elevation of cortical plasticity by valproic acid rapidly destabilizes the hierarchy of adult wildtype animals. These findings provide insight into mechanisms through which increased behavioral plasticity may be achieved to improve therapeutic recovery from psychiatric disorders that are associated with social deficits.

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Group housing and social dominance hierarchy affect circadian activity patterns in mice

Royal Society Open Science ◽

10.1098/rsos.201985 ◽

2021 ◽

Vol 8 (2) ◽

pp. 201985

Author(s):

Yuri Robbers ◽

Mayke M. H. Tersteeg ◽

Johanna H. Meijer ◽

Claudia P. Coomans

Keyword(s):

Social Environment ◽

Social Dominance ◽

Dominance Hierarchy ◽

Activity Patterns ◽

Dominance Rank ◽

Dominant Male ◽

Group Housing ◽

Male Mice ◽

Female Mice ◽

The Social

In this study, we investigated the effect of social environment on circadian patterns in activity by group housing either six male or six female mice together in a cage, under regular light–dark cycles. Based on the interactions among the animals, the social dominance rank of individual mice was quantitatively established by calculating Elo ratings. Our results indicated that, during our experiment, the social dominance hierarchy was rapidly established, stable yet complex, often showing more than one dominant mouse and several subordinate mice. Moreover, we found that especially dominant male mice, but not female mice, displayed a significantly higher fraction of their activity during daytime. This resulted in reduced rhythm amplitude in dominant males. After division into separate cages, male mice showed an enhancement of their 24 h rhythm, due to lower daytime activity. Recordings of several physiological parameters showed no evidence for reduced health as a potential consequence of reduced rhythm amplitude. For female mice, transfer to individual housing did not affect their daily activity pattern. We conclude that 24 h rhythms under light–dark cycles are influenced by the social environment in males but not in females, and lead to a decrement in behavioural rhythm amplitude that is larger in dominant mice.

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Resource variability and the collapse of a dominance hierarchy in a colour polymorphic species

Behaviour ◽

10.1163/1568539x-00003498 ◽

2018 ◽

Vol 155 (6) ◽

pp. 443-463 ◽

Cited By ~ 1

Author(s):

Dawson M. Brown ◽

Matthew S. Lattanzio

Keyword(s):

Social Dominance ◽

Dominance Hierarchy ◽

Environmental Variability ◽

Behavioural Flexibility ◽

Dominance Hierarchies ◽

Species Dominance ◽

Polymorphic Species ◽

Series Of Experiments ◽

Colour Morphs ◽

Resource Variability

Abstract Intraspecific social dominance hierarchies should be influenced by environmental variation; however, in colour polymorphic species, dominance hierarchies are often assumed fixed, and thus insensitive to environmental variability. We ran a series of experiments using the colour polymorphic long-tailed brush lizard (Urosaurus graciosus) to challenge this assumption. We staged contests between orange and yellow morph males over a single heated perch, two perches at the same temperature, or two perches differing in temperature. Our first experiment revealed that orange-throated males are socially dominant. However, this hierarchy collapsed in our other experiments as yellow males became more aggressive. Interestingly, both males only ever secured their own perch where the perches differed in temperature. These findings mirror observations of morph behavioural flexibility in nature and studies of behaviour–environment interactions in non-polymorphic taxa. We conclude that colour morphs may have an underappreciated ability to assess resource-level changes and respond with concomitant flexibility in behaviour.

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Epinephrine and Nor-Epinephrine Effects on Social Dominance Behavior

Psychological Reports ◽

10.2466/pr0.1970.27.2.195 ◽

1970 ◽

Vol 27 (2) ◽

pp. 195-198 ◽

Cited By ~ 2

Author(s):

Carl W. Lawrence ◽

Jack R. Haynes

Keyword(s):

Social Dominance ◽

Dominance Hierarchy ◽

Dominance Behavior ◽

Differential Effects ◽

Submissive Behavior ◽

The Social

Effects of epinephrine and nor-epinephrine on social dominance behavior in 24 male C57BL/6J mice were investigated. The social dominance hierarchy was created by placing pairs of Ss in a linear maze. The only way S could get to the goal box was by pushing the opposing S out. The dominant S pushed the submissive S out of the maze. After the dominance hierarchy was established, each S was placed in the dominance situation under each of the drug conditions, epinephrine and nor-epinephrine. The results showed that all conditions were significantly different from each other, with the greatest amount of dominance behavior being shown under nor-epinephrine and the greatest submissive behavior under epinephrine. It was concluded that epinephrine and nor-epinephrine may have differential effects on social dominance behavior.

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Dominance patterns and positional behaviour of sheep in yards

Animal Science ◽

10.1017/s0003356100022728 ◽

1974 ◽

Vol 19 (2) ◽

pp. 157-168 ◽

Cited By ~ 34

Author(s):

H. Dove ◽

R. G. Beilharz ◽

J. L. Black

Keyword(s):

Small Groups ◽

Social Dominance ◽

Voluntary Movement ◽

Dominance Hierarchy ◽

Dominance Status ◽

Linear Type ◽

Dominance Structure ◽

The Social ◽

Before And After ◽

Forced Movement

SUMMARY1. Observations were conducted to ascertain the social dominance structure in two small groups of castrated male Corriedale sheep. In these and a third group, the order of the sheep past a fixed point was recorded, when they were moving either voluntarily or under force. Records were also made of the way in which the sheep distributed themselves spatially in a confined area, relative to one or two men simulating yard work. In a fourth group divided into two sub-groups, the social dominance structure was determined before and after the subgroups were mixed, to assess the effect of mixing.2. The small groups showed a distinct social dominance hierarchy of a linear type, similar to that found in cattle and pigs. The dominance status of individual animals was correlated with their body weight, wither height and height at hocks. Dominance status within a subgroup remained stable following the mixing of sub-groups.3. The sheep adopted consistent positions in forced movement, and in relation to one or two men simulating yard work. There was no consistency in voluntary movement. Dominant animals did not lead the forced movement, were usually some distance from man, and were widely scattered from each other.4. Dominance status was closely related to positional behaviour.

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Dominance hierarchy formation in juvenile crayfish procambarus clarkii

Journal of Experimental Biology ◽

10.1242/jeb.202.24.3497 ◽

1999 ◽

Vol 202 (24) ◽

pp. 3497-3506 ◽

Cited By ~ 8

Author(s):

F.A. Issa ◽

D.J. Adamson ◽

D.H. Edwards

Keyword(s):

Positive Feedback ◽

Social Dominance ◽

Dominance Hierarchy ◽

Procambarus Clarkii ◽

Behavior Patterns ◽

Dominance Hierarchies ◽

Low Level ◽

Hierarchy Formation ◽

High Dominance ◽

Low Levels

The formation of social dominance hierarchies was studied in groups of five juvenile crayfish, 1.3-1.8 cm in length. Animals were grouped together in a small, featureless aquarium after having lived in isolation for more than a month. The occurrence of each of four behavior patterns (‘attack’, ‘approach’, ‘retreat’ and ‘escape’) was recorded for each animal, together with the frequency of encounters and the frequency of wins and losses. The frequencies of wins and losses were used to calculate the relative dominance value of each animal in the group. High levels of fighting developed immediately upon grouping the animals, and a positive feedback relationship between attacking and winning enabled one animal in each group to emerge quickly as the superdominant. If that animal was the largest, it remained as the superdominant; otherwise, it was replaced as superdominant within the first few days by the largest animal. This form of dominance hierarchy, with one superdominant and four subordinates, persisted throughout the duration of the grouping. Fighting declined over the first hour and by 24 h had dropped to low levels. After the first day, approaches were used together with attacks, and retreats replaced escapes. Attack and approach were the behavior patterns displayed most frequently by animals with high dominance values, whereas retreat and escape were performed by animals of low dominance. All these trends continued to develop over the next 2 weeks as the number of agonistic encounters declined to a low level.

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The effects of castration and androgen on the social dominance of BALB/cJ male mice

Physiological Psychology ◽

10.3758/bf03333000 ◽

1974 ◽

Vol 2 (1) ◽

pp. 93-98 ◽

Cited By ~ 9

Author(s):

C. T. Lee ◽

J. N. Naranjo

Keyword(s):

Social Dominance ◽

Male Mice ◽

The Social

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Social dominance hierarchy type and rank contribute to phenotypic variation within cages of laboratory mice

Scientific Reports ◽

10.1038/s41598-019-49612-0 ◽

2019 ◽

Vol 9 (1) ◽

Cited By ~ 13

Author(s):

Justin A. Varholick ◽

Alice Pontiggia ◽

Eimear Murphy ◽

Vanessa Daniele ◽

Rupert Palme ◽

...

Keyword(s):

Social Context ◽

Phenotypic Variation ◽

Social Dominance ◽

Dominance Hierarchy ◽

Phenotypic Traits ◽

Dominance Behavior ◽

Dominance Hierarchies ◽

Biologically Relevant ◽

Degree Of Dominance ◽

Relevant Factors

Abstract A tacit assumption in laboratory animal research is that animals housed within the same cage or pen are phenotypically more similar than animals from different cages or pens, due to their shared housing environment. This assumption drives experimental design, randomization schemes, and statistical analysis plans, while neglecting social context. Here, we examined whether a domain of social context—social dominance—accounted for more phenotypic variation in mice than cage-identity. First, we determined that cages of mice could be categorized into one of three dominance hierarchies with varying degrees of dominance behavior between cage-mates, and low levels of agonistic behavior in the home-cage. Most groups formed dynamic hierarchies with unclear ranks, contrasting with recent accounts of stable transitive hierarchies in groups of mice. Next, we measured some phenotypic traits, and found that social dominance (i.e. dominance hierarchy type and degree of dominance behavior) consistently accounted for some phenotypic variation in all outcome measures, while cage-identity accounted for phenotypic variation in some measures but virtually no variation in others. These findings highlight the importance of considering biologically relevant factors, such as social dominance, in experimental designs and statistical plans.

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Social aggression in an age-dependent dominance hierarchy

Behaviour ◽

10.1163/156853907781476436 ◽

2007 ◽

Vol 144 (7) ◽

pp. 753-765 ◽

Cited By ~ 13

Author(s):

Adam Cronin ◽

Jeremy Field

Keyword(s):

Social Dominance ◽

Dominance Hierarchy ◽

Conflicts Of Interest ◽

Social Rank ◽

Social Aggression ◽

Dominance Hierarchies ◽

Age Dependent ◽

The Relationship ◽

Animal Societies

AbstractSocial aggression arises from conflicts of interest over reproduction in animal societies. Aggression is often highly variable between individuals in a group, may be correlated with dominance, and is often integral to the establishment of dominance hierarchies that in turn determine reproductive opportunities. However, reproductive dominance is not always linked with social dominance: 'queens' are not always the most aggressive individuals in a group. Furthermore, in some animals social rank is determined without aggression, and derived through another means, such as gerontocracy. In such instances, what is the role of aggression, and what underlies the variation between individuals? Here, we investigate the relationship between inheritance rank and aggression in the hover wasp Liostenogaster flavolineata, which has an age-based inheritance queue. All females in this study were of known age and, thus, rank could be determined independently of behaviour. Observations of intra-colony aggression indicated that aggression increased with inheritance rank and occurred among non-breeding subordinates. This cannot be explained by models that do not account for aggression between non-breeders. It is likely that contests over inheritance rank and the higher future fitness anticipated by high-ranking individuals account for this pattern.

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