Research reportSocial interactions and 50 kHz ultrasonic vocalizations in adolescent and adult rats
Introduction
Human adolescents are at an increased risk of alcohol use. According to the 2006 Monitoring the Future National Survey, 6% of 8th graders, 19% of 10th graders and 30% of 12th graders reported being drunk within the past 30 days [21]. Similarly high levels of ethanol intake are seen in adolescents of other species, with adolescent rats, for instance, showing 2–3 times higher g/kg ethanol intake relative to their more mature counterparts [8], [14], [27], [55].
Interactions with peers are thought to be of principal importance for human adolescents, with individuals spending more time with peers during adolescence than at any other developmental period [19], [26]. Similarly, adolescent rats show high levels of social behavior, with these social interactions being essential for developing the ability to express and understand intraspecific communication signals [47]. Interactions with peers during adolescence provide a substantial source of positive experiences for humans [26], [28], and, in the same way, an opportunity to interact with peers is more rewarding for adolescent rats than for their more mature counterparts [15].
An important property of alcohol that contributes to adolescent drinking is its ability to facilitate certain forms of social behavior, particularly interactions with peers [2], [39]. For instance, adolescents at risk for extensive alcohol use strongly attribute to alcohol the property of enhancing their effectiveness in social situations [1]. This ethanol-induced social facilitation is not restricted to human adolescents. Acute exposure to relatively low experimental doses of ethanol (0.5–0.75 g/kg) administered intraperioneally (i.p.) has been shown to facilitate social interactions in group-housed adolescent rats tested under familiar, non-anxiogenic circumstances [40], [50], [51], with the effective dose even lower in socially deprived animals [53]. These doses produce blood ethanol concentrations (BECs) commensurate with the moderate (20–80 mg/dl) consumption range in humans [16].
Alcohol expectancy research indicates that heavy drinkers and/or problem drinkers strongly expect alcohol to make them more sociable and relaxed [6]. In human adolescents, expectancy for ethanol-induced social facilitation and their drinking experience might influence each other in a reciprocal, positive feedback fashion, with expectancies from drinking such as increased social confidence and comfort helping to produce those very consequences, and drinking experiences further reinforcing initial expectancies [39]. Therefore, adolescents may be particularly sensitive to ethanol-induced social facilitation due to ethanol-induced enhancement of the salience of social stimuli. Given that this important issue in alcohol research has not been addressed experimentally, the present study was designed to examine whether ethanol might increase hedonic value of social interactions more strongly in adolescent than in adult rats when indexed via assessment of 50 kHz ultrasonic vocalizations (USVs).
Under certain circumstances, USVs produced by rats have been used as a measure of affective states [see [25] for review]. Relatively long (300–3000 ms), low frequency (around 22 kHz) USVs are associated with negative affective states in rats [7], [37] since they are emitted by threatening or painful stimuli such as foot shock [44], predator odor [4], or lithium chloride administration [9], and are generated during defensive and submissive displays associated with inter-male fighting [42]. In contrast, shorter (20–80 ms) high frequency (around 50 kHz) USVs [5], [18] are seen in contexts involving potential reward, including play fighting [23], social exploration [5], male agonistic behaviors [36], and by males during sexual approach, copulation and ejaculation [32]. Increases in 50 kHz USVs are also seen in experimental situations, including tickling by the experimenter [11], [30], [35], electrical stimulation of the reward pathway and cues predicting such stimulation [10], amphetamine administration [22], [43], and cues associated with morphine administration [10]. These 50 kHz USVs are postulated to be an index of positive affective states in rats, given that they are increased in contexts involving appetitive stimuli [23], [24], [35]. The main objective of the present study was to determine the impact of ethanol administration on social affect in adolescent and adult male Sprague–Dawley rats using USV production as an index of the hedonic value of social interactions. The approach used was to examine production of 50 kHz USVs during social interactions following exposure to either saline or ethanol under dose and administration conditions previously shown to facilitate social interactions in adolescent rats [50], [51], [53].
Ethanol-induced changes in different components of social behavior and motivation for social contacts were also scored and analyzed. Thus a major goal of this study was to determine if 50 kHz USVs co-vary with the facilitation of social behavior by ethanol during adolescence [50], [51]. Although it has been shown that 50 kHz USVs correlate with dorsal contacts in pairs of isolate-housed adolescent rats [23], the relationship of USVs and social behaviors has yet to be studied in adult rats or among socially-housed adolescents exhibiting pharmacologically produced elevations in social interactions. Using a CPP paradigm, it has been previously shown that social stimuli are more rewarding for adolescent rats than adults, especially when the animals are housed in pairs [15]. A second goal of the present study was to further examine age differences in the rewarding value of social stimuli in both ethanol-treated and control animals.
Previous studies have shown that doses of ethanol in the social facilitatory range do not increase general locomotor activity in the social interaction test [50], [52], however it is unclear if these doses of ethanol may have motor activating properties in the absence of a social stimulus. To explore this issue, experimental subjects in this study were placed alone in the testing chamber daily for 5 min to analyze ethanol's effects on general locomotor activity.
Section snippets
Subjects
Sprague–Dawley male rats bred and reared in our colony at Binghamton University were used in this study. Female rats have been shown to emit differing levels of USVs dependent upon their estrous cycle [31], and therefore were not included in this experiment. A total of 96 rats derived from 24 litters were used. The day after birth, all litters were culled to 8–10 pups (6 males and 4 females when possible) and housed with their mother and father in standard breeding cages until weaning on
Locomotor activity
Ethanol had no impact on locomotor activity of experimental animals during the 5-min period prior to the onset of the social interaction test. As seen in Fig. 1 (data are collapsed across ethanol dose), in general, the number of crosses through the center aperture was significantly higher in adolescents than in adults [main effect of age, F(1,120) = 6.66, p < 0.005]. This age effect was tempered by test day [age × day interaction, F(3,120) = 8.00, p < 0.0001]. Overall locomotor activity of adolescent
Discussion
The results of the present study revealed pronounced age-related differences in 50 kHz USV production and social behavior. Adults exhibited more 50 kHz USVs while engaging in less social behavior relative to adolescents. Adolescent animals generally exhibited higher levels of social behaviors and showed ethanol-induced social facilitation of play fighting that was not evident in adults; this ethanol-induced social facilitation, however, was not accompanied by increases in 50 kHz USV production.
Acknowledgements
The research presented in this article was supported by grants from the National Institute of Health (R01 DA019071 and R01 AA016887) to Linda P. Spear and (R01 AA012453) to Elena I. Varlinskaya.
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2018, Physiology and BehaviorCitation Excerpt :Ethanol-induced social facilitation is not restricted to human adolescents but is also evident in adolescent rats [36]. Both male and female adolescent rats tested on P28-P35 under familiar, non-anxiety provoking circumstances show substantial increases in interaction with peers following acute exposure to relatively low doses of ethanol, an ethanol-induced facilitation of social behavior that is predominantly characterized by an increase in play behavior and is not normally seen in adults ([34,38,39,40,44]. Higher doses of ethanol have different social consequences, producing social inhibition, with male and female adolescent rats being less sensitive to these adverse social effects of ethanol than their more mature counterparts [40].
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2018, AlcoholCitation Excerpt :Indeed, ethanol-induced social facilitation is not restricted to human adolescents but can be seen in adolescent rats under normal circumstances (Varlinskaya & Spear, 2002). Young adolescent rats tested at postnatal day (P) 28 or 35 under familiar, non-anxiety provoking circumstances are uniquely sensitive to the socially activating effects of ethanol administered intraperitoneally (i.p.) in a low dose range (0.5–0.75 g/kg) on play fighting (Trezza, Baarendse, & Vanderschuren, 2009; Varlinskaya & Spear, 2002, 2006; Willey, Varlinskaya, & Spear, 2009), with this social facilitation normally not evident in older adolescents (P42) or adults (Varlinskaya & Spear, 2015). However, ethanol-induced facilitation of play fighting can be observed in older adolescents (Varlinskaya, Truxell, & Spear, 2013) and adults (Varlinskaya, Doremus-Fitzwater, & Spear, 2010) that demonstrate alterations in social responsiveness induced by repeated restraint stress.