Rats selectively bred for low levels of 50 kHz ultrasonic vocalizations exhibit alterations in early social motivation

Abstract

In rats, the rates of 50 kHz ultrasonic vocalizations (USVs) can be used as a selective breeding phenotype and variations in this phenotype can be an indicator of affective states. The 50 kHz USV is elicited by rewarding stimuli (e.g., food, sexual behavior) and therefore can express a positive affective state. Conversely, the 22 kHz USV is elicited by aversive stimuli (e.g., presence of a predator, social defeat) indicating a negative affective state. In the present study, we tested the effect of selectively breeding for 50 kHz USVs on a variety of maternal social/emotional behaviors in young rat pups (PND 10-12). These measures consisted of an assessment of isolation calls and conditioned odor preference paradigm. Results indicate that animals selected for low levels of 50 kHz USVs show the greatest alterations in social behaviors compared to the control animals. The low line animals had an increase in isolation calls tested during place preference conditioning and a decrease in 50 kHz ultrasonic calls in all conditions. These same low line animals failed to show a typical preference for a maternally-associated odor during the place preference test. The different social behaviors of the high line animals did not consistently vary from those of the control group. These results have important implications for the study of genetic and epigenetic mechanisms underlying emotional states, and possibly contribute to the research underlying the emotional changes in developmental disorders such as autistic spectrum disorder by providing a novel animal model that displays communication deficits that are interdependent with significant social behavioral impairments.

The effects of selective breeding for differential rates of 50‐kHz ultrasonic vocalizations on emotional behavior in rats

“…Conversely, animals bred for low rates of 50-kHz USVs exhibited both lower rates of 50-kHz USVs as well elevated rates of 22-kHz USVs compared to randomly bred animals (Burgdorf et al, 2005;Harmon et al, 2008). These data suggest that high line animals exhibit a greater dispositional tendency for positive affectivity and a lower dispositional tendency for negative affectivity.…”

“…In related work, low line animals failed to show a conditioned maternal preference (Harmon et al, 2008), using the procedures of Nelson and Panksepp (1996), whereas random and high line animals did show a maternal preference (Harmon et al, 2008). Therefore, it is possible that their lower social-motivation during adulthood reduces the likelihood of depressive responses (but their higher 22-kHz USVs would suggest increased susceptibility to depression).…”

“…Thus, the decrease in floating behavior seen in low line animals may reflect a heightened state of anxiety. Indeed, low line animals show higher levels of anxiety compared to the random line in the social interaction test (present study) and infant separation distress (Harmon et al, 2008). However, given that antidepressants also decrease rates of floating behavior in the Porsolt test (Cryan, Valentino, & Lucki, 2005) it is possible that low line animals are less prone to depression than random and high line animals.…”

“…The decrease in contact time in low line animals could also be interpreted as indicative of a decreased social reward, as measured by socially induced place preferences (Panksepp, Nelson, & Bekkedal, 1997). In related work, animals selectively bred for low levels of 50-kHz USVs showed higher rates of infant separation distress calls compared to the random line animals, which further suggests that the low line animals display a high anxiety phenotype (Harmon et al, 2008).…”

Prenatal Stress Alters the Development of Socioemotional Behavior and Amygdala Neuron Excitability in Rats

“…The pitch of USVs from control pups decreased with age, as previously reported (Kromkhun et al, 2013), but increased with age in PS pups, further suggesting atypical development following PS. Isolation-induced USVs are inherently social (Hofer et al, 2002;Harmon et al, 2008), and reductions of USVs have been found in rodent models of ASDs (Crawley, 2007;Higashida et al, 2011). Diminished USVs in rat pups are suggested to model the lack of crying observed in some children with ASDs (Crawley, 2007).…”