Maternal care, infant fear memory retention, and the moderating role of variations in separation‐induced ultrasonic vocalizations

Abstract

Individual differences in parental care predict variations in offspring anxiety across species. Here, we examined whether between‐ and within‐litter variations in maternal licking (a measure of rodent maternal care) predict infant rats’ retention of an aversive association (a predictor of later anxiety‐like behavior) and whether the relationship between maternal licking and infant fear memory is moderated by variations in infants’ solicitation of maternal care. Unique marks were drawn on each pup, coded for fading, and touched up daily across the first week of life. Mark fading was used as an index of maternal licking where greater fading suggested more maternal licking the previous day. Separation‐induced ultrasonic vocalizations (USVs) were recorded to measure individual differences in solicitation of maternal care. Infants were fear conditioned at postnatal day (P) 17 and tested for fear of the conditioned stimulus (CS) 1 week later. Across litters, mark fading negatively predicted CS‐elicited fear at test for male, but not female, offspring. This relationship was moderated by number of USVs emitted at P1, such that mark fading only predicted CS‐elicited fear for males that emitted a low number of USVs. These results suggest that offspring solicitation may moderate the relationship between maternal care and fear/anxiety.

Communal nesting shapes the sex-dependent glutamatergic response to early life stress in the rat prefrontal cortex

“…Importantly, as reported previously ( 35 ), pups reared in the CN condition emitted a lower number of USV when isolated from the nest at PND9, whereas no changes were observed in females, confirming the existence of sex-dependent differences in emotionality since the very first phases of life. Interestingly, these behavioral data are the first indication that male pups reared in a socially enriched environment (i.e., CN), known to represent a naturalistic setting able to induce stress resilience ( 25 ), might better cope to subsequent challenging events, as suggested by their reduced USV at PND9 and increased pinning during adolescence ( 47 , 48 ).…”

Minimizing Variability in Developmental Fear Studies in Mice: Toward Improved Replicability in the Field

“…The majority of studies analyzing rodent fear behavior in development have a blinded experimenter manually score freezing across the whole behavioral session (Carew & Rudy, 1991; Colon et al., 2018; Glavonic et al., 2023; Pattwell et al., 2012; Revillo et al., 2016; Revillo, Paglini, & Arias, et al., 2014). As this can be quite labor‐intensive, a subset of studies uses a time‐sampling approach, in which a binary freezing/no freezing category is assigned to a particular time interval of 3 s (Baker & Richardson, 2015; Bisby et al., 2018; Harmon‐Jones & Richardson, 2021; Kim et al., 2009, 2011; Kim & Richardson, 2007a,b, 2008; McCallum et al., 2010; Yap & Richardson, 2007; Zimmermann et al., 2023), 5 s (Cain et al., 2003; Hefner & Holmes, 2007), or 10 s (Kutlu et al., 2018; Morgan & Pfaff, 2001). Although manual scoring is time‐consuming and may carry the possibility of observer bias, it allows for quantification of complex behaviors that might be difficult to score automatically (such as grooming and rearing, as in Colon et al., 2018, but see below).…”

Infant ultrasonic vocalizations predict adolescent social behavior in rats: Effects of early life adversity

“…Behaviors displayed during separation from the mother can provide information about the affective state of the infant or the motivation to solicit maternal care and have been proposed as predictive of later‐life behavior in both humans and nonhuman animal models (Schwartz et al., 1999; Zimmerberg et al., 2005). In rodents, isolation‐induced ultrasonic vocalizations (USVs) have been interpreted as a sign of separation distress in infants (Branchi et al., 2001; Brudzynski, 2021) as well as solicitation of maternal care (Harmon‐Jones & Richardson, 2021; Wöhr & Schwarting, 2008); when isolated from the dam, infant rats emit USVs in the 40 kHz range, which serve as a signal to the dam to initiate maternal behavior (Brouette‐Lahlou et al., 1992; Ehret & Haack, 1981). Both higher‐than‐typical and lower‐than‐typical USV emission during isolation have been associated with temperaments that predict anxiety‐like and social behaviors later in life (Brunelli et al., 2006).…”