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Mouse Ethogram: Barbering Behavior

By November 16, 2019January 23rd, 2022No Comments

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Definition

Barbering, often referred to as the Dalila effect, is a grooming behavior displayed by a mouse on itself or other cagemates which involves the plucking of fur, hairs, or whiskers.

Description

Barbering is of interest to neurobehavioral research because it is an activity that is very common in rodent waking life. Barbering is an aggressive behavior in which one mouse aggressively grooms itself or another mouse, resulting in the removal of fur and/or whiskers. In some strains of mice, such as the NMRI strain, barbering may be associated with fighting, thus it’s an agonistic behavior.

Barbering, when performed by one mouse on another, is believed to serve the purpose of establishing dominance and hierarchy.

Barbering may also be an abnormal behavior when the mouse is observed obsessively plucking itself, as is the case in self-plucking.

Social Barbering is Triggered by Crowded Group Housing Conditions

In crowded and dense housing conditions, social barbering is expressed in junction with anxiety. Therefore, barbering can indicate that mice are subjected to stressful housing conditions.

Behavioral Variants Associated with Barbering

Barbering has several variations:

Self-Plucking

During self-plucking, the mouse aggressively plucks its own fur, whiskers, or hair.

During this type of barbering, the most commonly affected and barbered areas of the body are the cheek, the inside/outside of the forearms, and the genitals.

Cage-Mate Plucking

In cage-mate plucking, also known as “social barbering” or “hetero-barbering,” one mouse will barber another mouse. The areas between the ears, rump, dorsal face or neck, and/or whiskers are commonly affected by this barbering behavior.

The recipient of the barbering behavior is often seen flinching, a response that is not observed in allogrooming which is a different behavior that is associated with fur and grooming but is interpreted as being more positive and building social bonds.

Whisker-Picking

Some researchers highlight ‘whisker-picking’ as a specific type of barbering in their studies and score this as a separate category. Whisker-picking is when only the whiskers (vibrissae) and the adjacent hairs of one mouse are plucked by another mouse.

Function of Barbering

Barbering is a complex behavior that is commonly observed in the lab. Since barbering is an abnormal behavior in the context of self-plucking, its function is still not fully understood. However, the following functions are applicable in terms of social barbering:

  • To establish and exert dominance. Social barbering is commonly exerted in order to establish dominance status over other mice. In fact, dominant mice are likely to barber other cage mates which are not as dominant. If a dominant mouse is barbered, it does not alter their inherent levels of social dominance.
  • To protect its territory. Related to the previous point of establishing and exerting dominance, mice will use barbering when protecting their territory as one of the behaviors elicited during confrontational encounters with intruding mice. By barbering, a mouse can weaken another mouse and decrease its chances of intruding again.

By exerting dominance and achieving higher hierarchical status within the group, a mouse can be better off, since dominance is associated with better access to resources without the constant need to enter intense fights.

Applications of Barbering

Barbering can be observed under certain circumstances, including:

  • During a territorial threat. If a mouse is confronted by an unknown mouse and perceives the encounter to be a territorial threat, barbering may occur as a part of the subsequent agonistic behaviors between the two mice.
  • Within the presence of subordinate animals. If a mouse is more dominant, it will barber other subordinate mice in order to establish and/or reinforce dominance within the colony. Therefore, the presence of weaker mice may trigger cagemate plucking as performed by the more dominant mouse.
  • During allogrooming. Sometimes, when mice are engaging in allogrooming behaviors, barbering may occur. Thus, the presence of other mice combined with the grooming context may trigger barbering.

Behavioral Tests for Measuring Barbering

Barbering can be measured and quantified in many ways, including:

  • Video analysis. In a grouped-housing situation, barbering will be observed and the behavior is usually captured and measured through video recording and analysis. By recording, a mouse colony can be observed across time and behaviors such as barbering can be quantified more easily than by having an observer.
  • The Tube Dominance Test. When assessing dominance in a confrontational setting between two mice, cagemate or social barbering may be exhibited during the Tube Dominance Test. Two mice are placed in a single tube from each end and can only move forwards, since the tube is narrow and not spacious. Thus, the only way to reach the other side is to move forward and be confrontational towards the other mouse. Dominance is a trait that is directly correlated with completing the Tube Dominance Test which ends as soon as one mouse makes it to the other side.
  • The Resident-Intruder Test. In this test, when an unknown mouse is placed in the cage in which a single mouse resides, an agonistic encounter is extremely likely to occur. In this case, barbering may be performed by the more dominant mouse.

Pharmaceutical Findings on Barbering

Barbering is a behavior that can be affected by pharmaceutical administration. However, not many studies exist which test the effects of drugs on this behavior.

Clomipramine Reduces Barbering in Trichotillomania Mice

Clomipramine is a tricyclic antidepressant that is able to inhibit the serotonin reuptake system. Mice with a genetic mutation that knockouts the nitric oxide synthase (NOS2) gene are used as an animal model of trichotillomania due to their high levels of barbering behavior. However, when given clomipramine, these mice will barber significantly less after 10-20 days of treatment when compared with untreated NOS2 mice. More information will be given about NOS2 mice in the upcoming Mouse Strains section.

Estradiol Injections Reduce Barbering in Trichotillomania Mice

Trichotillomania, defined as repetitive hair-plucking, is related to Obsessive-Compulsive Disorder and is a common disorder in women. Yet, not much is known regarding the disorder’s mechanisms and biological causes. In mice, barbering is a hair-plucking behavior that has been validated as a model for trichotillomania. Correlations have been found between the onset of trichotillomania and changes in reproductive physiology, leading to the hypothesis that reproductive hormones may play a role in the disease. Estrogen doses are able to influence the brain’s catecholamines and endogenous opiates which are known to regulate and interact with corticostriatal loops which are implicated in motor and planning behavior. Both estrogen and the corticostriatal loops are aspects of cognition that are known to be affected in patients with trichotillomania. Thus, injections of estrogen are bound to affect barbering (which is a behavior that may model trichotillomania in mice). In fact, estradiol, which is an estrogen steroid hormone, is able to modify barbering behavior in mice.17β-estradiol benzoate injections reduce barbering in females when compared to females on a vehicle solution. The effect of estrogen injections implies that sex hormones are critical for determining the onset of trichotillomania.

Mouse Strains Exhibiting Barbering Behavior

Barbering can be observed across many mouse strains at varying frequencies. Some strains may display high levels of barbering while other strains display low levels of barbering.

NMRI Mice

NMRI mice have been used in behavioral research for almost a century now for general studies as well as for pharmacology or toxicology. NMRI mice are commonly used as a control or comparator breed but as they increase in age they may develop tumors spontaneously or even renal disease.

Social barbering will be exhibited by NMRI mice even if they are housed together since weaning. Social barbering is common in the NMRI mice for both males and females. However, in same-sex cages, barbering is also associated with fighting in males, but not in females.

If NMRI mice are socially housed together for the first time, barbering will still be observed within 2-5 days of grouping. Barbering within this strain is characterized by head and snout denuding, as well as whisker removal.

C57BL/6 Mice and Barbering

C57BL/6 mice will begin to demonstrate social barbering at about 14 weeks of age. At 20 weeks of age, this strain will begin to demonstrate whisker-plucking specifically if housed in pens containing 8 mice or more. In general, C57BL/6 mice are regarded as a strain which demonstrates high levels of barbering and are usually used as a comparator strain in behavioral studies.

129S1 Mice

129S1/SvImJ mice, simply referred to as 129S1 mice, are commonly used as a background strain in behavioral research (as C57Bl/6 mice are) and are known for their anxiety-like behavioral tendencies and learning variabilities. Furthermore, 129S1 mice are also popular in behavioral research as they can be easily used to produce targeted mutations because they have multiple embryonic stem cell lines available.

When it comes to barbering, 129S1 female mice are more likely to exhibit social barbering behaviors amongst each other than males under housing conditions which include group housing since weaning.

BALB/cJ Mice

BALB/cJ male mice will begin to demonstrate whisker-picking at 10 weeks old, while female BALB/cJ mice begins at 12 weeks old (on average). This suggests a possible gender difference between BALB/cJ male and female mice with respect to the first manifestation of barbering behavior.

PLCβ1 Knockout Mice

Schizophrenic patients have been reported to have reduced levels of phospholipase C (PLC) β1 in certain regions of the brain. In general, phospholipids, which are affected by this type of genetic abnormality, have an important neuro-architectural role since phospholipids are necessary for the structure of neural  membranes and efficient signal transduction which connect neuronal response and receptor occupancy. In humans, PLCβ1 has been found to be expressed in the hippocampus, cerebral cortex, amygdala, olfactory bulb, and lateral septum. Mice that have the PLCβ1 gene knocked out may share some similar abnormalities with patients with schizophrenia, including inhibition of the acoustic startle response and hyperactivity in the Open Field. These mice also have social abnormalities including low levels of sociability and low instances of barbering. Low levels of barbering is considered to be an abnormality since barbering is associated with the establishment of a social hierarchy. Thus, the lack of barbering (and thus, by extension, probably lack of hierarchy) is a peculiarity which may further reflect the schizophrenic phenotype described by a lack of social skills as expressed by social withdrawal and isolation.

A2G Mice

Barbering is found to increase in incidence within the A2G mice as they age. One experiment, conducted by Strozik and Festing, established that in about 75% of the cages which have 2-3 mice, there will be at least 1 active barber by the time that the mice become 60 days old. In cages with male mice, usually, there is one mouse with untrimmed whiskers, presumably the most dominant of the male mice. In contrast, several female mice are likely to be barbers within a cage. Current evidence is pointing in the direction that female A2G mice are sensitive to pregnancy and are less likely to be whisker-plucked by their cage mates if they are pregnant.

AChe-/-

Acetylcholinesterase (AChE) is known to function in nerve impulse transmission and may even serve as a cell adhesion factor when there is neurite outgrowth occurring. This would theoretically imply that mice without AChE would not be able to live. However, AChE-/- knockout mice are, in fact, born alive and can survive for an average of 14 days. When these mouse strains are fed with a high fat diet, their lifespan can increase anywhere from 100 days to 15 months. Male mice that are fed on this diet will not be threatening or demonstrate aggression, but they will establish hierarchy and barber one another’s whiskers and fur across the face, shoulders, and back.

NOS2 Knockout Mice

NOS2 knockout mice lack the nitric oxide synthase gene and have high levels of barbering as a result. Having nitric oxide synthase knocked out consequently reduces the microtubule-associated protein 2 levels in PC12 cells. Also, since nitric oxide is involved in regulating glutamate, its deletion affects the neurotransmitter as well as the migration and maturation of the cortex’s neurons. This mouse strain has limited neuronal maturation which may ultimately lead to inadequate inhibition of the brain’s motor programs leading to the inability to stop trimming or barbering. These mice will demonstrate barbering in high instances by the time they become 4 weeks old and will continue to increase in the amount that they perform barbering by the time they reach adulthood.

GalNAc-4-ST1–/– mice

GalNAc-4-ST1–/– mice have a genetic mutation which ultimately affect their luteinizing hormone (LH). LH is an important hormone since it is crucial for the proper production of sex hormones testosterone, estradiol, and progesterone. Therefore, any perturbation with this hormone can be associated with issues in sexual development and maturity. The structure of LH is such there is has a unique N-linked carbohydrate unite which ends with a sulfated N-acetylgalactosamine structure (GalNAc-4-SO4)  which is important for clearing LH from the blood. In order to target this, researchers ablate the gene that encodes the sulfotransferase which is involved in adding the sulfate to the GalNAc found on the LH. In mice, this corresponds to the GalNAc-4-sulfotransferase-1 (GalNAc-4-ST1).

GalNAc-4-ST1-/- mice have very high levels of barbering amongst one another. Since this genetically manipulated strain also has higher levels of testosterone than normal, they demonstrate early sexual maturation and higher aggressive behavior which is observed in the form of higher instances of barbering.

S-COMT Deficient Mice

Catechol-O-methyltransferase (COMT) is responsible for catalyzing or breaking down the O-methylation of important catecholic compounds that are found in the brain, such as L-dopa, catecholamines, and also their hydroxylated metabolites. COMT is an enzyme that has two forms, soluble (S-COMT) or membrane-bound (MB-COMT) isoforms. Both are known to be products which come from the same gene. In rodents and in humans alike, S-COMT is more available but in the human brain, there is about a 2.5-fold higher amount of MB-COMT than S-COMT. It has been found that mice that lack both forms of COMT have a two-fold increase of the time it takes to eliminate dopamine from the prefrontal cortex. In S-COMT deficient mice, it has been established that subtle social interaction changes occur. These include increase in barbering behavior, as well as decreased sniffing time of another mouse.

Abnormalities of Barbering

Schizophrenia

Schizophrenia is associated with altered barbering levels. Mice that model schizophrenia are likely to have barbering affected. For example, PLCβ1 mice have low levels of barbering and this is an abnormality because barbering is associated with the natural establishment of a social hierarchy. Thus, the lack of barbering (and thus, by extension, probably lack of hierarchy) is a peculiarity which may further reflect the schizophrenic phenotype described by a lack of social skills as expressed by social withdrawal and isolation.

Trichotillomania

Trichotillomania is an abnormality of barbering since it is classified as an impulse control disorder that specifically affects grooming. Mice with this abnormality exhibit excessive fur trimming and pulling, ultimately leading to abnormally high levels of barbering.

Disease Models Exhibiting Barbering Behavior

Trichotillomania Mouse Model

Trichotillomania is an impulse control disorder which is commonly studied in behavioral research since it is estimated to affect 1-3.5% of the human population. Trichotillomania is characterized by the urge for hair trimming or pulling and can be modeled in mice either through genetic induction or spontaneously.

Spontaneous Trichotillomania Within Mouse Colonies

In 2004, the mouse model of trichotillomania was developed. An epidemiological study conducted by Garner et al. observed the behavior of over 2,950 laboratory mice, in order to assess the face validity of this model, and concluded that when mice begin to barber spontaneously, they can serve as experimental animals which model the disease.

Barbering is a complicated behavior which may arise as a result of multiple variables, from genetic, to social, to stress-evoked reactions.

Genetically Induced Trichotillomania

NOS2 knockout mice also serve as a genetic model of trichotillomania. These mice display high levels of barbering behavior, and as described earlier, have nitric oxide synthase knocked out which consequently reduces the microtubule-associated protein 2 levels in PC12 cells. Also, nitric oxide is involved in regulating glutamate research and the migration and maturation of the cortex’s neurons. This mouse strain has limited neuronal maturation which may ultimately lead to inadequate inhibition of the brain’s motor programs leading to the inability to stop trimming or barbering. Since trichotillomania and obsessive-compulsive disorder, in general, are associated with the malfunction of the cortico-striato-thalamo-cortical circuitry, it makes sense to observe such behavioral abnormalities.

Barbering Affects Cognition and Behavioral Performance

A recent experiment demonstrated that mice with plucked off whiskers perform differently in behavioral tests than mice that have their whiskers intact.

In the Tube Dominance Test, a trend was detected showing that whiskered mice were more dominant than whiskerless mice. However, future research must expand on this with a larger sample size.

Another trend was detected in the Paired Interaction Test. The non-whiskered mice spent less time investigating their partner than whiskered mice did. Also, the whiskerless mice spent significantly more time in vertical rearings, less time strewing and digging the litter material in the cage and less time cleaning their bodies.

Finally, in the Forced Swim Test, whiskered mice were significantly more active during the first two minutes of the test than whiskerless mice meaning that whiskered mice have higher levels of active behavioral avoidance.

Given these differences, researchers should consider the state of the mice’s whiskers prior to an experiment since plucked off whiskers are potentially indicative of underlying behavioral problems.

Research Tip: How to handle barbering within a laboratory setting

Since barbering may be observed during behavioral research, it is important to know how to handle barbering and have some ideas as to what you should do if you observe barbering amongst your mice.

When exaggerated barbering or grooming leads to bald spots or even, as observed in severe situations, open sores, then it is important to isolate the injured mouse. Otherwise, an injured mouse with an open sore can trigger more aggressive attacks to occur which may ultimately lead to the death of the injured mouse. After isolating the mouse until its wound closes and hair regrows, it can be reintroduced into a group cage.

If you observe three or four barbered mice and one unbarbed mouse, consider removing the unbarbered mouse which is probably the most dominant of the group.

Summary

  • Barbering is a behavior displayed by a mouse on itself or other cagemates which involves the plucking of fur, hairs, or whiskers.
  • Barbering is also known as the Dalila effect.
  • Barbering can be classified as an aggressive or agonistic behavior.
  • In other cases, barbering may be an abnormal behavior.
  • There are several variants of barbering behavior, including self-plucking, cage-mate plucking, and whisker-picking.
  • Social barbering is triggered by crowded group housing conditions.
  • The functions of social barbering are to establish dominance and to protect one’s territory.
  • Under the following scenarios, barbering can be observed: during a territorial threat, within the presence of subordinate animals, and during allogrooming.
  • The following behavioral tests can be used in some way to measure barbering behavior in mice: video analysis, the Tube Dominance Test, and the Resident-Intruder Test.
  • Pharmaceutical studies have been useful in establishing how drugs can attenuate barbering in mice. The following have been established:
    • Clomipramine reduces barbering in trichotillomania mice.
    • Estradiol injections reduce barbering in trichotillomania mice.
  • Many mouse strains have been found to exhibit barbering. The following findings demonstrate how barbering varies across mouse strains:
    • Social barbering will be exhibited by NMRI mice even if they are housed together since weaning.
    • C57BL/6 mice will begin to demonstrate social barbering at about 14 weeks of age.
    • 129S1 female mice are more likely to exhibit social barbering behaviors amongst each other than males.
    • BALB/cJ male mice will begin to demonstrate whisker-picking at 10 weeks old, while female BALB/cJ mice begin at 12 weeks old (on average).
    • Schizophrenic mice (PLCβ1 knockout mice) have social abnormalities including low levels of sociability and low instances of barbering.
    • Barbering is found to increase in incidence within the A2G mice as they age.
    • NOS2 knockout mice lack the nitric oxide synthase gene and have high levels of barbering as a result.
  • Schizophrenia and trichotillomania are abnormalities that have led to alterations in barbering behavior in mice.
  • Barbering can influence behavioral assessment, thus researchers that observe barbering behavior should take extra care.

References

  1. http://web.stanford.edu/~jeromeg/cgi-bin/Barbering.php
  2. http://mousebehavior.org/barbering/
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  4. Sarna, Justyna R., Richard H. Dyck, and Ian Q. Whishaw. “The Dalila effect: C57BL6 mice barber whiskers by plucking.” Behavioural brain research 108.1 (2000): 39-45.
  5. Kalueff, A. V., et al. “Hair barbering in mice: implications for neurobehavioural research.” Behavioural processes 71.1 (2006): 8-15.
  6. Horii, Yasuyuki, et al. “Hierarchy in the home cage affects behaviour and gene expression in group-housed C57BL/6 male mice.” Scientific reports 7.1 (2017): 6991.
  7. Garner, Joseph P., et al. “Barbering (fur and whisker trimming) by laboratory mice as a model of human trichotillomania and obsessive-compulsive spectrum disorders.” Comparative medicine 54.2 (2004): 216-224.
  8. Tur, M. A., and I. V. Belozertseva. “Effect of Spontaneous Partial Sensory Deprivation on the Behavior of Male C57BL/6N Mice.” Neuroscience and Behavioral Physiology(2018): 1-7.
  9. Casarotto, Plinio C., et al. “Inducible nitric oxide synthase (NOS2) knockout mice as a model of trichotillomania.” PeerJ 6 (2018): e4635.
  10. Husk, Sarah Elizabeth Hess. “The role of estrogen in the onset and performance of plucking behavior in a mouse model of trichotillomania.” (2010).
  11. Koh, H‐Y., et al. “Deficits in social behavior and sensorimotor gating in mice lacking phospholipase Cβ1.” Genes, Brain and Behavior 7.1 (2008): 120-128.
  12. Strozik, E., and M. F. W. Festing. “Whisker trimming in mice.” Laboratory animals 15.4 (1981): 309-312.
  13. Duysen, Ellen G., et al. “Rescue of the acetylcholinesterase knockout mouse by feeding a liquid diet; phenotype of the adult acetylcholinesterase deficient mouse.” Developmental brain research 137.1 (2002): 43-54.
  14. Mi, Yiling, Dorothy Fiete, and Jacques U. Baenziger. “Ablation of GalNAc-4-sulfotransferase-1 enhances reproduction by altering the carbohydrate structures of luteinizing hormone in mice.” The Journal of clinical investigation 118.5 (2008): 1815-1824.
  15. Tammimäki, Anne, et al. “Effect of S-COMT deficiency on behavior and extracellular brain dopamine concentrations in mice.” Psychopharmacology 211.4 (2010): 389-401.
  16. Coleman, Ruth A., et al. “A practical method of chronic ethanol administration in mice.” Alcohol. Humana Press, 2008. 49-59.
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