Tickling during adolescence alters fear-related and cognitive behaviors in rats after prolonged isolation

Hori, Manabu; Yamada, Kazuo; Ohnishi, Junji; Sakamoto, Sadao; Furuie, Hiroki; Murakami, Kazuo; Ichitani, Yukio

doi:10.1016/j.physbeh.2014.04.008

Cited by 16 publications

(6 citation statements)

References 37 publications

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“…Reported effects of rat tickling at the genetic and cellular level include altered gene expression in the hypothalamus 37 , and increased neurogenesis in the dentate gyrus of the hippocampus 38 39 . Outcomes indicative of reduced generalized anxiety and fear of humans are also reported such as reduced latency to approach in 9 different experiments 13 , less freezing after fear conditioning 40 41 , and increased entries into the center of an open field arena by individually housed rats 36 . For further information see LaFollette et al , who present a systematic review of the tickling literature that identifies 22 reports investigating the outcomes of rat tickling in comparison to other techniques 13 .…”

Section: Representative Resultsmentioning

confidence: 94%

Tickling, a Technique for Inducing Positive Affect When Handling Rats

Cloutier

LaFollette

Gaskill

et al. 2018

JoVE

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Handling small animals such as rats can lead to several adverse effects. These include the fear of humans, resistance to handling, increased injury risk for both the animals and the hands of their handlers, decreased animal welfare, and less valid research data. To minimize negative effects on experimental results and human-animal relationships, research animals are often habituated to being handled. However, the methods of habituation are highly variable and often of limited effectiveness. More potently, it is possible for humans to mimic aspects of the animals' playful rough-and-tumble behavior during handling. When applied to laboratory rats in a systematic manner, this playful handling, referred to as tickling, consistently gives rise to positive behavioral responses. This article provides a detailed description of a standardized rat tickling technique. This method can contribute to future investigations into positive affective states in animals, make it easier to handle rats for common husbandry activities such as cage changing or medical/research procedures such as injection, and be implemented as a source of social enrichment. It is concluded that this method can be used to efficiently and practicably reduce rats' fearfulness of humans and improve their welfare, as well as reliably model positive affective states.

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Section: Representative Resultsmentioning

confidence: 94%

Tickling, a Technique for Inducing Positive Affect When Handling Rats

Cloutier

LaFollette

Gaskill

et al. 2018

JoVE

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“…Among these, 71% (n = 5) found fewer anxiety and fear behaviors in tickled rats. Three distinct positive results were found: decreased freezing after fear conditioning [22, 26], increased locomotor activity and entries into the center of an open field arena [23], and increased entries and time in the open arms of an elevated plus maze by high-callers only on day 2 of testing [27]. However, elevated plus maze behavior was unaffected by tickling in two other studies [4, 20].…”

Section: Resultsmentioning

confidence: 99%

“…However, elevated plus maze behavior was unaffected by tickling in two other studies [4, 20]. Additionally, no behavioral changes due to tickling treatments were observed in a Forced Swim Test [27], Cat Odor Test [4], Flinch-Jump Test [26], or Morris water maze [26]. …”

Section: Resultsmentioning

confidence: 99%

Rat tickling: A systematic review of applications, outcomes, and moderators

et al. 2017

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IntroductionRats initially fear humans which can increase stress and impact study results. Additionally, studying positive affective states in rats has proved challenging. Rat tickling is a promising habituation technique that can also be used to model and measure positive affect. However, current studies use a variety of methods to achieve differential results. Our objective was to systematically identify, summarize, and evaluate the research on tickling in rats to provide direction for future investigation. Our specific aims were to summarize current methods used in tickling experiments, outcomes from tickling, and moderating factors.MethodsWe systematically evaluated all articles about tickling identified from PubMed, Scopus, Web of Science, and PsychInfo. Our inclusion criteria were publication in a peer-reviewed journal and collection of original, empirical data on rats using the handling method of tickling. One researcher extracted information from each article. Bias was assessed by 2 investigators using the SYRCLE bias assessment tool.ResultsWe identified 32 articles (56 experiments) published in peer-reviewed journals about rat tickling for inclusion. A wide variety of strains, sexes, and ages of rats were included. The most common method used for tickling was cycling through 15 seconds of tickling and 15 seconds of rest for 2 minutes for 3 to 5 days. Experiments with a control for tickling (N = 22) showed that tickling increases positive vocalization, approach behavior, decreases anxiety measures, improves handling, and in some cases decreases stress hormones. Tickling juvenile, individually housed rats with a trait predisposition to respond more positively to tickling, results in the most positive outcomes. Methods to reduce bias were insufficiently reported.ConclusionsWe conclude that tickling is a promising method for improving rat welfare and investigating positive affect. However, the establishment of tickling best practices is essential as the outcomes from tickling can be moderated by several factors.

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“…During domestication processes of wild animals, development of affiliative behavior toward humans has often been associated with reduced levels of anxiety 47,48 . Tickling during developmental periods has been reported to decrease anxiety-related behavior in rats in adulthood 54,55 . However, we previously found that post-weaning www.nature.com/scientificreports/ stroked groups of male rats show no significant difference in anxiety-related behavior 28 .…”

Section: Discussionmentioning

confidence: 99%

Post-weaning stroking stimuli induce affiliative behavior toward humans and influence brain activity in female rats

Okabe

Takayanagi

Yoshida

et al. 2021

Sci Rep

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Gentle touch contributes to affiliative interactions. We investigated the effects of gentle stroking in female rats on the development of affiliative behaviors toward humans and we exploratively examined brain regions in which activity was influenced by stroking. Rats that had received stroking stimuli repeatedly after weaning emitted 50-kHz calls, an index of positive emotion, and showed affiliative behaviors toward the experimenter. Hypothalamic paraventricular oxytocin neurons were activated in the rats after stroking. The septohypothalamic nucleus (SHy) in the post-weaningly stroked rats showed decreased activity in response to stroking stimuli compared with that in the non-stroked control group. There were negative correlations of neural activity in hypothalamic regions including the SHy with the number of 50-kHz calls. These findings revealed that post-weaning stroking induces an affiliative relationship between female rats and humans, possibly via activation of oxytocin neurons and suppression of the activity of hypothalamic neurons.

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Tickling during adolescence alters fear-related and cognitive behaviors in rats after prolonged isolation

Cited by 16 publications

References 37 publications

Tickling, a Technique for Inducing Positive Affect When Handling Rats

Tickling, a Technique for Inducing Positive Affect When Handling Rats

Rat tickling: A systematic review of applications, outcomes, and moderators

Post-weaning stroking stimuli induce affiliative behavior toward humans and influence brain activity in female rats

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