Elsevier

Physiology & Behavior

Volume 87, Issue 3, 30 March 2006, Pages 527-536
Physiology & Behavior

The effects of selective breeding for infant ultrasonic vocalizations on play behavior in juvenile rats

https://doi.org/10.1016/j.physbeh.2005.11.020Get rights and content

Abstract

For over 25 generations, two lines of rats (High and Low USV lines) have been selectively bred for extreme rates of infantile (45 kHz) ultrasonic vocalizations (USV) in response to maternal separation at postnatal day (P)10. High and low line juveniles (P30–P40) were socially isolated and allowed to play in same-sex sibling pairs for 10 min per day over three days. Measures of play were nape contacts and pinning. Other social and nonsocial behaviors were also scored during the three sessions; two of these, 55 kHz USV and walk-overs, were statistically associated with play. Compared to the Random control line, both High and Low line juveniles showed deficits in play behavior. In the High line, play initiatory behavior (nape contacts) was reduced, but pinning, USV and walk-overs were relatively unchanged. In contrast, nape contacts, pinning, USV and walk-overs were all reduced in Low line juveniles compared to Random line controls. The results suggest that selection for extremes of infant USV rates has produced temperamental differences that are expressed in juvenile play in the High and Low USV lines.

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)

  • S.M. Siviy et al.

    The relative playfulness of juvenile Lewis and Fischer-344 rats

    Physiol Behav

    (2003)
  • B. Zimmerberg et al.

    Differences in affective behaviors and hippocampal allopregnanolone levels in adult rats of lines selectively bred for infantile vocalizations

    Behav Brain Res

    (2005)
  • J.M. van Ree et al.

    Low doses of beta-endorphin increase social contacts of rats tested in dyadic encounters

    Life Sci

    (1983)
  • S.M. Pellis et al.

    What do rats find rewarding in play fighting? — An analysis using drug induced play partners

    Behav Brain Res

    (1995)
  • L.J.M.J. Vanderschuren et al.

    The neurobiology of social play behavior in rats

    Neurosci Biobehav Rev

    (1997)
  • B. Knutson et al.

    High-frequency ultrasonic vocalizations index conditioned pharmacological reward in rats

    Physiol Behav

    (1999)
  • A.J. Wintink et al.

    The related roles of dopamine and glutamate in the initiation of 50 kHz ultrasonic calls in adult rats

    Pharm Biochem Behav

    (2001)
  • K. Choong et al.

    Prenatal ethanol exposure alters the postnatal development of the spontaneous electrical activity of dopamine neurons in the ventral tegmental area

    Neurosci

    (2004)
  • K. Muneoka et al.

    Prenatal nicotine exposure affects the development of central serotonergic as well as dopaminergic system in rat offspring: involvement of route of drug administrations

    Dev Brain Res

    (1997)
  • A.C. Grobin et al.

    Regulation of the prefrontal cortical dopamine system by the neuroactive steroid 3α-OH-5α-pregnan-20-one

    Brain Res

    (1992)
  • B. Zimmerberg et al.

    Prenatal experience and postnatal stress modulate the adult neurosteroid and catecholaminergic stress responses

    Int J Dev Neurosci

    (1998)
  • E.F. Field et al.

    Differential effects of amphetamine on attack and defense components of play fighting in rats

    Physiol Behav

    (1994)
  • G.J. Hole et al.

    Play in rodents

  • J. Panksepp

    The ontogeny of play in rats

    Dev Psychobiol

    (1981)
  • S.M. Pellis

    Agonistic versus amicable targets of attack and defense: consequences for the origin, function, and descriptive classification of play-fighting

    Aggress Behav

    (1988)
  • Cited by (0)

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