Involvement of orexin/hypocretin in the expression of social play behaviour in juvenile rats

Reppucci, Christina J.; Gergely, Cassandra K.; Bredewold, Remco; Veenema, Alexa H.

doi:10.1080/21594937.2020.1720132

Cited by 11 publications

(10 citation statements)

References 94 publications

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“…We confirmed previous findings that males have higher extracellular glutamate, but not GABA, concentrations in the LS compared to females, resulting in a higher glutamate/GABA ratio in males under baseline conditions as well as during exposure to the social play test (Bredewold et al, 2015). Despite this sex difference, males and females show similar levels of social play behavior in our testing conditions (current study; Veenema et al, 2013;Bredewold et al, 2014Bredewold et al, , 2015Bredewold et al, , 2018Reppucci et al, 2018Reppucci et al, , 2020. We now show that LS-V1aR blockade abolished the sex difference in extracellular glutamate concentrations as well as in glutamate/GABA ratio under baseline conditions and during exposure to the social play test.…”

Section: Discussionsupporting

confidence: 91%

Vasopressin regulates social play behavior in sex-specific ways through glutamate modulation in the lateral septum

Bredewold

Washington

Veenema

2023

Preprint

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Social play is a highly rewarding behavior that is essential for the development of social skills. Social play is impaired in children diagnosed with autism, a disorder with a strong sex bias in prevalence. We recently showed that the arginine vasopressin (AVP) system in the lateral septum (LS) regulates social play behavior sex-specifically in juvenile rats: Administration of a AVP 1a receptor (V1aR) antagonist increased social play behavior in males and decreased it in females. Here, we demonstrate that glutamate, but not GABA, is involved in the sex-specific regulation of social play by the LS-AVP system. First, males show higher extracellular glutamate concentrations in the LS than females while they show similar extracellular GABA concentrations. This resulted in a baseline sex difference in excitatory/inhibitory balance, which was eliminated by V1aR antagonist administration into the LS: V1aR antagonist increased extracellular glutamate release in females but not in males. Second, administration of the glutamate receptor agonist L-glutamic acid into the LS prevented the V1aR antagonist-induced increase in social play behavior in males while mimicking the V1aR antagonist-induced decrease in social play behavior in females. Third, administration of the glutamate receptor antagonists AP-5 and CNQX into the LS prevented the V1aR antagonist-induced decrease in social play behavior in females. Last, both sexes showed increases in extracellular LS-GABA release upon V1aR antagonist administration into the LS and decreases in social play behavior upon administration of the GABA-A receptor agonist muscimol into the LS, suggesting that GABA is not involved in the sex-specific regulation of social play by the LS-AVP system. Finally, to start identifying the cellular mechanism mediating the sex-specific effects of the LS-AVP system on LS-glutamate, we determined the presence of potential sex differences in the type of LS cells expressing V1aR. However, no sex differences were found in the percentage of Avpr1a+ LS cells expressing markers for either GABAergic neurons, somatostatin-expressing neurons, calbindin 1-expressing neurons, or astrocytes. In conclusion, these findings demonstrate that the LS-AVP system regulates social play sex-specifically via differential local glutamatergic neurotransmission in male and female juvenile rats. Further research is required to uncover the underlying cellular mechanism.

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Section: Discussionsupporting

confidence: 91%

Vasopressin regulates social play behavior in sex-specific ways through glutamate modulation in the lateral septum

Bredewold

Washington

Veenema

2023

Preprint

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“…A more practical approach is to test selected pairs of rats in a neutral arena, as this creates a test trial that is convenient to the experimenter (Panksepp, 1981). For example, the timing of the trial can be crucial in pharmacological studies where the rats need to be tested when the drugs have maximal effects (e.g., Achterberg et al., 2014; Field & Pellis, 1994; Reppucci, Gergely, Bredewold, & Veenema, 2020). To increase their motivation to engage in play at the time selected by the experimenter, the rats can be socially isolated prior to testing (Hole, 1991a).…”

Section: Conducting Play Trialsmentioning

confidence: 99%

Measuring Play Fighting in Rats: A Multilayered Approach

et al. 2022

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Rough-and-tumble play or play fighting is an important experience in the juvenile period of many species of mammals, as it facilitates the development of social skills, and for some species, play fighting is retained into adulthood as a tool for assessing and managing social relationships. Laboratory rats have been a model species for studying the neurobiology of play fighting and its key developmental and social functions. However, play fighting interactions are complex, involving competition and cooperation; therefore, no single measure to quantify this behavior is able to capture all its facets. Therefore, in this paper, we present a multilayered framework for scoring all the relevant facets of play that can be affected by experimental manipulations and the logic of how to match what is measured with the question being asked.

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“…Alternatively, we have previously observed individual and/or cohort variability in social investigation by young rats in other behavioral paradigms [8,10,33,34]. Thus, despite some cohort variability, as a whole, males and females exhibited similar patterns of stimulus preference and levels of stimulus investigation in the Social versus Food Preference Test under all examined conditions.…”

Section: Males and Females Exhibited Similar Stimulus Preferences Amentioning

confidence: 63%

Wistar rats and C57BL/6J mice differ in their motivation to seek social interaction versus food in the Social versus Food Preference Test

Reppucci

Brown

Chambers

et al. 2020

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Here we characterized the Social versus Food Preference Test, a behavioral paradigm designed to investigate the competition between the choice to seek social interaction versus the choice to seek food. We assessed how this competition was modulated by internal cues (social isolation, food deprivation), external cues (time-of-testing, stimulus salience), sex (males, females), age (adolescents, adults), and rodent model (Wistar rats, C57BL/6J mice). We found that changes in stimulus preference in response to the internal and external cue manipulations were similar across cohorts. Specifically, social over food preference scores were reduced by food deprivation and social familiarly in Wistar rats and C57BL/6J mice of both sexes. Interestingly, the degree of food deprivation-induced changes in stimulus investigation patterns were greater in adolescents compared to adults in Wistar rats and C57BL/6J mice. Strikingly, baseline stimulus preference and investigation times varied greatly between rodent models: across manipulations, Wistar rats were generally more social-preferring and C57BL/6J mice were generally more food-preferring. Adolescent Wistar rats spent more time investigating the social and food stimuli than adult Wistar rats, while adolescent and adult C57BL/6J mice investigated the stimuli a similar amount. Neither social isolation nor time-of-testing altered behavior in the Social versus Food Preference Test. Together, our results indicate that the Social versus Food Preference Test is a flexible behavioral paradigm suitable for future interrogations of the peripheral and central systems that can coordinate the expression of stimulus preference related to multiple motivated behaviors.Running Head: SOCIAL VS. FOOD 3 HIGHLIGHTS  Rats prefer social over food when sated, and this is attenuated by food deprivation.  Mice have no preference when sated, and prefer food over social when food-deprived.  Rats prefer a familiar social stimulus or a novel social stimulus over food.  Mice prefer food over a familiar social stimulus.  Adolescent rats investigate social and food stimuli longer than adult rats. GRAPHICAL ABSTRACTRunning Head: SOCIAL VS. FOOD

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Involvement of orexin/hypocretin in the expression of social play behaviour in juvenile rats

Cited by 11 publications

References 94 publications

Vasopressin regulates social play behavior in sex-specific ways through glutamate modulation in the lateral septum

Vasopressin regulates social play behavior in sex-specific ways through glutamate modulation in the lateral septum

Measuring Play Fighting in Rats: A Multilayered Approach

Wistar rats and C57BL/6J mice differ in their motivation to seek social interaction versus food in the Social versus Food Preference Test

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