Effects of neonatal handling on play and anxiety in F344 and Lewis rats

Siviy, Stephen M.

doi:10.1002/dev.21622

Cited by 5 publications

(5 citation statements)

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“…Based on this data, an experimental paradigm known as “neonatal handling” was developed, in which rodent pups are briefly separated from their mothers for the first 3 weeks of life and exposed to a new environment ( Levine et al, 1956 ; Papaioannou et al, 2002 ; Raineki et al, 2014 ). The NH effects include changes in hypothalamic-pituitary-adrenal axis function, improvement in the organism’s ability to cope with stress, and reducing anxious behavior (reduced emotionality; Papaioannou et al, 2002 ; Raineki et al, 2014 ; Siviy, 2018 ). At the same time, NH leads to ambiguous changes in learning and memory depending on the task, and negatively affects social behavior in early and adult life ( Papaioannou et al, 2002 ; Raineki et al, 2014 ).…”

Section: Discussionmentioning

confidence: 99%

“…The classic NH procedure consists of placing pups separately from the dams in a new environment for 3 min and repeating this procedure daily with PND 1–20 ( Raineki et al, 2014 ). The parameters of this model vary across studies in terms of the time of pup separation (1–15 min), number of exposure days and pups may also be exposed to additional stimuli during separation (e.g., grooming with a soft brush; Papaioannou et al, 2002 ; Garoflos et al, 2008 ; Bock et al, 2011 ; Zhang et al, 2012 ; Raineki et al, 2014 ; Akatsu et al, 2015 ; Siviy, 2018 ). In our experiment, the pups were subjected to various daily experimental manipulations during the first 3 weeks after birth, which included separating them from their mothers and transferring them to a new environment for testing.…”

Section: Discussionmentioning

confidence: 99%

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The Behavior and Postnatal Development in Infant and Juvenile Rats After Ultrasound-Induced Chronic Prenatal Stress

et al. 2021

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Fetal development is susceptible to environmental factors. One such factor is exposure to stress during pregnancy. The present study aimed to investigate the effects of chronic prenatal stress (PS) on the development and behavior of rat offspring during infancy and juvenile ages. Existing approaches to modeling prenatal stress on animals do not correlate with the main type of stress in pregnant women, namely psychological stress. We used a new stress paradigm in the experiment, namely, stress induced by exposure to variable frequency ultrasound (US), which acted on pregnant Wistar rats on gestational days 1–21. This type of stress in rodents can be comparable to psychological stress in humans. We assessed physical development, reflex maturation, motor ability development, anxious behavior, response to social novelty, and social play behavior in male and female offspring. Additionally, we investigated maternal behavior and the effect of neonatal handling (NH) on behavior. Prenatal stress did not affect postnatal developmental characteristics in rat pups, but prenatally stressed rats had higher body weight in early and adult age than controls. Prenatal exposure to a stressor increased anxiety in the open-field test (OF), changed social preferences in the social novelty test (SN), and impaired social play behavior in males. Neonatal handling reduced anxiety and restored social behavior, but evoked hyperactive behavior in rat pups. Maternal behavior did not change. Our study demonstrated for the first time that exposure to variable frequency ultrasound during pregnancy influences offspring development and impairs behavior, correlating with the effects of other types of stress during pregnancy in rodents. This supports the idea of using this exposure to model prenatal stress.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

The Behavior and Postnatal Development in Infant and Juvenile Rats After Ultrasound-Induced Chronic Prenatal Stress

et al. 2021

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“…On the other hand, when rats are tested for a discrete period (e.g. 5-15 min) in a neutral testing chamber with unfamiliar rats after a period of social isolation, sex differences are less likely to be observed (Himmler et al 2013(Himmler et al , 2014Siviy 2018). As the rats in the present study were tested with an unfamiliar partner after a brief period of social isolation, robust sex differences in play would not be expected.…”

Section: Discussionmentioning

confidence: 62%

Individual differences in social play behaviour predict alcohol intake and control over alcohol seeking in rats

et al. 2021

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Rationale Social play behaviour is a rewarding social activity displayed by young mammals, thought to be important for the development of brain and behaviour. Indeed, disruptions of social play behaviour in rodents have been associated with cognitive deficits and augmented sensitivity to self-administration of substances of abuse, including alcohol, later in life. However, the relation between social development and loss of control over substance use, a key characteristic of substance use disorders including alcohol use disorder (AUD), has not been investigated. Moreover, it remains unknown how inherent differences in playfulness relate to differences in the sensitivity to substance use and AUD. Objective The objective of this study is to determine how individual differences in juvenile social play behaviour predict alcohol intake and loss of control over alcohol seeking. Methods Juvenile male Lister hooded rats were characterized for their tendency to engage in social play behaviour. Subsequently, alcohol consumption and conditioned suppression of alcohol seeking were assessed in the tertiles of rats that showed the most and least social play. Results The rats that engaged most in social play behaviour consumed more alcohol than their less playful counterparts. However, whereas the most playful rats showed intact conditioned suppression of alcohol seeking, the least playful rats showed no such suppression. Conclusion Individual levels of playfulness predict the sensitivity to alcohol-directed behaviour. Highly playful rats are more prone to alcohol intake, yet show greater control over alcohol seeking. These findings increase our understanding of the relationship between social development and vulnerability to AUD.

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“…For instance, gentle handling of adolescent rats improved learning and memory and decreased anxiety, measured in the elevated plus‐maze test (Costa et al, 2012). Moreover, neonatal handling is beneficial for rodents in many aspects, such as reducing anxiety levels and bizarre behaviors, improving cognition and increasing playful responsiveness (Baeta‐Corral & Giménez‐Llort, 2014; Siviy, 2018). Neonatal handling decreases anxiety and stress response in rats in two‐way active avoidance test by significantly reducing the hippocampus and amygdala volumes (Río‐Álamos et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

“…Results from elevated plus maze test, which is used to test the levels of anxiety of rodents, indicate that rats that have been gently handled before the test have decreased anxiety levels, which results in improved learning and memory (Boix et al, 1988;Costa et al, 2012;Fern andez-Teruel et al, 1991). The same effect of handling has been observed in neonatal rodents, in fear-motivated tests such as the afore-mentioned active avoidance, among others (Muntsant et al, 2019;Río-Alamos et al, 2017;Siviy, 2018).…”

Section: Introductionmentioning

confidence: 89%

Handling and novel object recognition modulate fear response and endocannabinoid signaling in nucleus basalis magnocellularis

Tena

Moreno‐Rodríguez

Llorente-Ovejero

et al. 2022

Eur J of Neuroscience

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Storage of aversive memories is of utmost importance for survival, allowing animals to avoid upcoming similar stimuli. However, without reinforcement, the learned avoidance response gradually decreases over time. Although the molecular mechanisms controlling this extinction process are not well known, there is evidence that the endocannabinoid system plays a key role through CB1 receptor‐mediated modulation of cholinergic signaling. In this study, we measured fear extinction throughout 7 months using naïve rats, assessed in passive avoidance (PA) test in a non‐reinforced manner. Then, we evaluated the effect of gentle handling and non‐aversive novel object recognition test (NORT) on the extinction and expression of fear memories by measuring passive avoidance responses. Neurochemical correlates were analyzed by functional autoradiography for cannabinoid, cholinergic, and dopaminergic receptors. Despite results showing a gradual decrease of passive avoidance response, it did not fully disappear even after 7 months, indicating the robustness of this process. Meanwhile, in rats that received gentle handling or performed NORT after receiving the PA aversive stimulus, extinction occurred within a week. In contrast, gentle handling performed before receiving the aversive stimulus exacerbated fear expression and triggered escape response in PA. The neurochemical analysis showed increased cannabinoid and cholinergic activity in the nucleus basalis magnocellularis (NBM) in rats that had performed only PA, as opposed to rats that received gentle handling before PA. Additionally, a correlation between CB1 mediated‐signaling in the NBM and freezing in PA was found, suggesting that the endocannabinoid system might be responsible for modulating fear response induced by aversive memories.

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Effects of neonatal handling on play and anxiety in F344 and Lewis rats

Cited by 5 publications

References 62 publications

The Behavior and Postnatal Development in Infant and Juvenile Rats After Ultrasound-Induced Chronic Prenatal Stress

The Behavior and Postnatal Development in Infant and Juvenile Rats After Ultrasound-Induced Chronic Prenatal Stress

Individual differences in social play behaviour predict alcohol intake and control over alcohol seeking in rats

Handling and novel object recognition modulate fear response and endocannabinoid signaling in nucleus basalis magnocellularis

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