Effects of Genetic Background, Gender, and Early Environmental Factors on Isolation-Induced Ultrasonic Calling in Mouse Pups: An Embryo-Transfer Study

Abstract

Infant rodents emit ultrasonic vocalizations when isolated from dam and littermates. Due to the context of their occurrence and the well described bidirectional modulation by substances known for their capability to influence emotionality, it was postulated that such calls reflect a negative affective state akin anxiety. Comparative studies observed pronounced differences in calling behavior between strains, which were paralleled by differences in maternal care. Therefore, it was recently hypothesized that early environmental factors may have strong impact on call production. Here, the relative contributions of genetic background, gender, and early environmental factors on calling behavior in C57BL/6JOlaHsd and C57BL/6NCrl were studied by using an embryo-transfer procedure. The results show that these sub-strains differ in the amount of calling and specific call features, like call frequency and amplitude. The embryo-transfer procedure indicated that the observed differences in the amount of ultrasonic calling are dependent on the dyadic interaction between mother and pup. Conversely, call features were primarily dependent on the genotype of the pup. Thus, call frequency and frequency modulation were solely dependent on the pup, i.e. its genotype and gender. However, there was one exception, namely call amplitude, which was solely dependent on the genotype of the mother, i.e. on early environmental factors. Furthermore, it was shown that particularly changes in call amplitude might be of high functional relevance, since a sub-strain dependent preference towards pups emitting calls with high amplitudes was observed. In total, it can be concluded that both genomic and nongenomic factors can tune calling behavior in mouse pups.

Altered ultrasonic vocalizations in a tuberous sclerosis mouse model of autism

“…The possible maternal impacts on vocalization may be broadly classified into prenatal versus postnatal effects. Prenatal effects include possibilities as diverse as imprinting of genes inherited maternally, metabolic defects that affect gestational development, or immune responses to the pups during pregnancy (24). Environ-mental stimuli are known to influence vocalization rates, including changes in handling, litter size, and fostering (25,27), and differences in maternal care might affect the environment in which pups are raised and subsequently influence their vocalization rates.…”

Rodent ultrasonic communication and its relevance for models of neuropsychiatric disorders

“…In mice, we found similar effects. By conducting an embryo-transfer study, we showed that the isolation-induced calling behaviour in infant mice is highly dependent on early environmental factors such as maternal care [41]. We found that even the closely related mouse strains C57BL/6JOla and C57BL/6N differ in USV production in isolation.…”

Ultrasonic vocalizations in house mice:

“…Interestingly, the sex and developmental stage of offspring influences maternal retrieval behaviours (male pups receive more maternal care than females, and more-developed pups are retrieved sooner than less-developed individuals) (Hahn and Lavooy, 2005), something that may be explained by differences in the calling rate of infant male and female mice (Hahn et al, 1998). Interestingly, maternal responsiveness of a mouse strain is negatively correlated with pup USV calling rate, indicating a close linkage of these behaviours in lab strains (D'Amato et al, 2005;Wöhr et al, 2008). This interaction of maternal response rates and offspring USV production suggests the potential for parent-offspring conflicts, which could be a fruitful area for future research (Box 10.3).…”

“…A crossfostering study on laboratory mice pups revealed that call features were primarily dependent on the genotype of the pup, and call amplitude was the only feature dependent on the maternal genotype, i.e. on early environmental factors (Wöhr et al, 2008). Another cross-fostering study with BALB and B6 mice, which show strain-specific call types, revealed that adult courtship calls of fostered males remained similar to calls of their genetic parental strain, and did not copy their fostered parents (Kikusui et al, 2011).…”