The effects of selective breeding for infant ultrasonic vocalizations on play behavior in juvenile rats
Introduction
Social play is characteristic of most preadolescent (juvenile) mammals, including nonhuman primates and humans [1]. In rats, play appears at about postnatal day 18, increases until it peaks between roughly 30 and 40 days, and then slowly declines with the onset of puberty after about 40 days of age [2], [3]. In younger juvenile rats (under 30 days) play occurs spontaneously among animals in close proximity, whereas older animals (30–45 days) initiate play fights [4].
A variety of intrinsic and extrinsic factors affect the frequency and quality of play, as well as subsequent development of social behavior. Among intrinsic factors, pre- and postnatal neuroendocrine events produce sexual differentiation of play in male and female rats [5], [6], [7], [8]. Prenatal stressors of various kinds reduce play in juvenile rats [9], [10], and later environmental enrichment can sometimes reverse these effects [9]. Prenatal alcohol exposure has been reported to reduce pinning and nape contact during juvenile play, but to cause more sniffing, chasing, hopping and darting [11], and to increase overall levels of play-fighting [12]. Prenatal cocaine suppresses levels of play, rendering juvenile offspring less likely to pin or be pinned, and to pounce or be pounced upon [13], [14].
Both pre- and postnatal malnutrition significantly reduce play behaviors in juvenile rats [15], [16], leaving non-playful social behavior (allogrooming and anogenital sniffing) intact. Finally, social behavior in adults and play in juveniles are known to vary by rat strain, indicating underlying genetic variation in levels of playfulness [17], [18], [19], [20], [21].
To address the development of temperamental differences across the lifespan, we have selectively bred the High and Low USV lines rats based on rates of infant 45 kHz USV emission to 2 min of separation and isolation at postnatal day (P)10 [22], [23], [24]. The High and Low lines have diverged extensively in their USV rates from each other and from the Random line, which has maintained the original progenitor N:NIH strain rates across many generations (Fig. 1).
In creating the High and Low selectively bred lines the goal was to produce central nervous system differences regulating emotional reactivity, based on the quantitative differences in the infant USV response to separation. As infants, High line pups eliminate (defecate/urinate) more, an indication of greater autonomic reactivity associated with “emotionality” in adult rats [25], [26], [27]. In adulthood High line rats show significantly more behavioral indices of anxiety and depression than the Low line in response to novelty or laboratory stressors such as open field emergence, novel social interaction and the Porsolt forced swim task [28]. Yet both the High and Low USV lines show enhanced cardiac responses to novelty as juveniles and to restraint stress in adulthood: the High line via greater sympathetic activation of heart rate, and the Low line through profound withdrawal of normal parasympathetic restraint on heart rate [29], [30]. Thus, the two selected lines each provide a unique model of temperamental biases in reactivity to novelty and stress from infancy into adulthood.
What has not been examined in the lines, however, are the effects of selective breeding for infantile USV on social behavior in juveniles and adults. As a first step, the present investigation examines the question of whether selective breeding for high and low USV rates has affected common indices of juvenile play behavior, and vocalizations associated with play [31].
Section snippets
Subjects
All procedures used in this study were reviewed and approved by the New York State Psychiatric Institute's Institutional Animal Care and Use Committee. Subjects were postnatal (P) 30–37 day-old male and female juvenile sibling pairs from High, Random, and Low line litters from the 25th and 26th selected generations. Subjects had not been tested as infants for USV rates. Twelve High (6 female; 6 male), 15 Low (8 females; 7 male), and 13 Random (7 female; 6 male) sibling pairs of juveniles
Results
Table 1 shows the average age of juveniles at the first habituation, and average weights of male and female sibling pairs at three time points. The age of juveniles was not different by lines or sexes (p > .6 and .9, respectively), with no interactions. Not surprisingly, juveniles' average weights were correlated with their ages across the age range (r[78] = .681, p = .001). Next, the effects of line, sex and age at habituation were tested across the three weight measures. A significant line effect (F
Discussion
The results of this study demonstrate that selective breeding for either high or low USV rates at P10 has reduced frequencies of play behaviors (napes, pins and USVs). It is noteworthy that play behaviors were reduced exclusively, ruling out global deficits in social behavior, locomotor abilities or differences in arousal. The only other behavior affected in the lines was walk-overs, which is associated with play in juveniles [15]. The High line showed significant deficits only in nape contacts
References (51)
- et al.
A descriptive study of social development in the rat (Rattus norvegicus)
Anim Behav
(1981) Hormonal organization of sex differences in play fighting and spatial behavior
The sexual differentiation of social play
TINS
(1988)- et al.
Prenatal stress potentiates stress-induced behavior and reduces the propensity to play in juvenile rats
Physiol Behav
(1992) - et al.
Effects of alcohol exposure during development on social behavior in rats
Physiol Behav
(2003) - et al.
Prenatal cocaine exposure: effects on play behavior in the juvenile rat
Neurotoxicol Teratol
(1994) - et al.
Play behavior and stress responsivity in periadolescent offspring exposed prenatally to cocaine
Pharmacol Biochem Behav
(1995) - et al.
Prenatal malnutrition affects the social interactions of juvenile rats
Physiol Behav
(1996) - et al.
Postnatal protein malnutrition affects play behavior and other social interactions in juvenile rats
Physiol Behav
(2001) - et al.
Rough-and-tumble play behavior in Fischer-344 and Buffalo rats: effects of isolation
Physiol Behav
(1997)