Deficits in Burrowing Behaviors Are Associated With Mouse Models of Neuropathic but Not Inflammatory Pain or Migraine

Shepherd, Andrew J.; Cloud, Megan E.; Cao, Yu Qing; Mohapatra, Durga P.

doi:10.3389/fnbeh.2018.00124

Cited by 35 publications

(37 citation statements)

References 43 publications

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“…The analysed faecal samples were collected 12 days after the onset of the respective handling, which might have been a sufficient time frame to adapt to the handling stress for all males and the daily handled females, but not for the weekly handled females. We think it is particularly noteworthy that, although the FCM concentrations of males were not influenced by handling technique or handling frequency, we confirm significant stress-associated affective and wellbeing associated impairments with an increase in the despair behaviour 56,57 and a reduced burrowing in the home cage 29,58 , while females remained unaffected regarding behaviours in these domains. This supports the fact that in most murine models females exhibit less anxiety in behavioural tests than males 59 .…”

Section: Discussionsupporting

confidence: 54%

The impact of handling technique and handling frequency on laboratory mouse welfare is sex-specific

Sensini

Inta

Palme

et al. 2020

Sci Rep

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Handling is a well-known source of stress to laboratory animals and can affect variability of results and even compromise animal welfare. The conventional tail handling in mice has been shown to induce aversion and anxiety-like behaviour. Recent findings demonstrate that the use of alternative handling techniques, e.g. tunnel handling, can mitigate negative handling-induced effects. Here, we show that technique and frequency of handling influence affective behaviour and stress hormone release of subjects in a sex-dependent manner. While frequent tail handling led to a reduction of wellbeing-associated burrowing and increased despair-like behaviour in male mice, females seemed unaffected. Instead, they displayed a stress response to a low handling frequency, which was not detectable in males. This could suggest that in terms of refinement, the impact in handling could differ between the sexes. Independently from this observation, both sexes preferred to interact with the tunnel. Mice generally explored the tunnel more often than the tail-handling hands of the experimenter and showed more positively rated approaches, e.g. touching or climbing, and at the same time, less defensive burrowing, indicating a strong preference for the tunnel.

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Section: Discussionsupporting

confidence: 54%

The impact of handling technique and handling frequency on laboratory mouse welfare is sex-specific

Sensini

Inta

Palme

et al. 2020

Sci Rep

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“…However, such evoked-pain tests are neither ethologically relevant to rodents, nor model experience of human chronic pain ( Rice et al, 2008 ). Consequently, innate rodent behaviors, such as burrowing, digging and nest-building that seek to mirror human activities of daily living have been explored as pain assays ( Deacon, 2006 ; Jirkof, 2014 ; Shepherd et al, 2018 ). A decrease in burrowing behavior has been used to assess pain-like behavior after CFA-induced knee inflammation in rats ( Rutten et al, 2014 ) and digging is a similar innate behavior that is quick and easy to test in a laboratory ( Deacon, 2006 ).…”

Section: Discussionmentioning

confidence: 99%

Acute inflammation sensitizes knee-innervating sensory neurons and decreases mouse digging behavior in a TRPV1-dependent manner

et al. 2018

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Ongoing, spontaneous pain is characteristic of inflammatory joint pain and reduces an individual's quality of life. To understand the neural basis of inflammatory joint pain, we made a unilateral knee injection of complete Freund's adjuvant (CFA) in mice, which reduced their natural digging behavior. We hypothesized that sensitization of knee-innervating dorsal root ganglion (DRG) neurons underlies this altered behavior. To test this hypothesis, we performed electrophysiological recordings on retrograde labeled knee-innervating primary DRG neuron cultures and measured their responses to a number of electrical and chemical stimuli. We found that 24-h after CFA-induced knee inflammation, knee neurons show a decreased action potential generation threshold, as well as increased GABA and capsaicin sensitivity, but have unaltered acid sensitivity. The inflammation-induced sensitization of knee neurons persisted for 24-h in culture, but was not observed after 48-h in culture. Through immunohistochemistry, we showed that the increased knee neuron capsaicin sensitivity correlated with enhanced expression of the capsaicin receptor, transient receptor potential vanilloid 1 (TRPV1) in knee-innervating neurons of the CFA-injected side. We also observed an increase in the co-expression of TRPV1 with tropomyosin receptor kinase A (TrkA), which is the receptor for nerve growth factor (NGF), suggesting that NGF partially induces the increased TRPV1 expression. Lastly, we found that systemic administration of the TRPV1 antagonist, A-425619, reversed the decrease in digging behavior induced by CFA injection, further confirming the role of TRPV1, expressed by knee neurons, in acute inflammatory joint pain.

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“…Unfortunately, few studies have directly compared these measures. 52,69,95,126,128 An important appeal of burrowing as an outcome measure of pain is that it requires simple equipment and is relatively easy to implement. Observations are easily performed in the home cage, reducing potential interference from stress, and methods employing latency to begin burrowing, burrowing duration and total volume displaced have been described.…”

Section: Burrowing Behaviorsmentioning

confidence: 99%

“…Burrowing represents a goal-directed behavior that laboratory mice and rats are motivated to perform, and the technique can be applied as a research tool, as well as for clinical assessment. 29,30,32,34,129,131 While it can be used to specifically assess pain, 3,12,46,52,59,61,69,95,111,[124][125][126]128,130,145,147 reductions in burrowing activity can also identify the influence of a range of factors, not all of which may be associated with pain, such as cognitive dysfunction, anxiety, systemic bacterial and viral infections, and inflammation. 24,27,29,[31][32][33][34]47,55,57,98,144 As such, burrowing may be viewed as a surrogate measure of pain in rodents, and also as a reflection of instrumental activities of daily living (IADL), an outcome used in humans to reflect the impact of disabilities such as pain on day-to-day activities (for example, general mobility, care of others, maintaining the living space).…”

Section: Burrowing Behaviorsmentioning

confidence: 99%

A Review of Pain Assessment Methods in Laboratory Rodents

2019

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Ensuring that laboratory rodent pain is well managed underpins the ethical acceptability of working with these animals in research. Appropriate treatment of pain in laboratory rodents requires accurate assessments of the presence or absence of pain to the extent possible. This can be challenging some situations because laboratory rodents are prey species that may show subtle signs of pain. Although a number of standard algesiometry assays have been used to assess evoked pain responses in rodents for many decades, these methods likely represent an oversimplification of pain assessment and many require animal handling during testing, which can result in stress-induced analgesia. More recent pain assessment methods, such as the use of ethograms, facial grimace scoring, burrowing, and nest-building, focus on evaluating changes in spontaneous behaviors or activities of rodents in their home environments. Many of these assessment methods are time-consuming to conduct. While many of these newer tests show promise for providing a more accurate assessment of pain, most require more study to determine their reliability and sensitivity across a broad range of experimental conditions, as well as between species and strains of animals. Regular observation of laboratory rodents before and after painful procedures with consistent use of 2 or more assessment methods is likely to improve pain detection and lead to improved treatment and care—a primary goal for improving overall animal welfare.

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Deficits in Burrowing Behaviors Are Associated With Mouse Models of Neuropathic but Not Inflammatory Pain or Migraine

Cited by 35 publications

References 43 publications

The impact of handling technique and handling frequency on laboratory mouse welfare is sex-specific

The impact of handling technique and handling frequency on laboratory mouse welfare is sex-specific

Acute inflammation sensitizes knee-innervating sensory neurons and decreases mouse digging behavior in a TRPV1-dependent manner

A Review of Pain Assessment Methods in Laboratory Rodents

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