Early Life Maternal Separation and Maternal Behaviour Modulate Acoustic Characteristics of Rat Pup Ultrasonic Vocalizations

Abstract

Early separation of preterm infants from their mothers has adverse, long-term neurodevelopmental consequences. We investigated the effects of daily maternal separation (MS) of rat pups from postnatal days 2–10 (PND2–10) on neurobehavioural responses to brief isolation at PND12 compared with pups receiving controlled handling without MS. Ultrasonic vocalizations (USV) were measured at PND12 during two, 3-minute isolations occurring immediately before and after a 3-minute maternal reunion. There were no significant differences in acoustic characteristics between MS and control animals in the first isolation. However, in the second isolation, MS pups produced a greater proportion of high (~60 kHz) vs low (~40 kHz) frequency calls. During this isolation, control pups made longer and louder low frequency calls compared to the first isolation, whereas MS pups did the opposite. Maternal behaviour of control and MS mothers modulated pup acoustic characteristics in opposite directions; higher maternal care was associated with more low frequency calls in control pups but more high frequency calls in MS pups. We hypothesize that MS results in USV emission patterns reflective of a greater stress response to isolation. This translational model can be used to identify mechanisms and interventions that may be exploited to overcome the negative, long-term effects of MS.

Biological Functions of Rat Ultrasonic Vocalizations, Arousal Mechanisms, and Call Initiation

“…Moreover, rats selected for higher emotionality traits emitted more ultrasonic calls when isolated as compared to pups with lower emotionality [ 45 ]. With the prolonged separation of pups from their mother, the acoustic parameters of their vocalization changed, and the pups emitted a larger proportion of high sound frequencies than the controls [ 46 , 47 ].…”

Maternal separation affects fronto-cortical activity in rat pups during dam-pup interactions and behavioral transitions

“…This procedure was based on a well-established paradigm consisting of pup isolation, brief reunion with dam, and a second isolation during which rates of USV production are increased over the rates during the initial isolation (Hofer et al, 2002). Methods and USV related findings have been described elsewhere (Kaidbey et al, 2019). Briefly, between 10 am and 12 pm, 30-minutes be-fore testing, the dam was removed from the home cage and brought to a novel room in a cage with fresh bedding, water and food.…”

“…Our separation paradigm was based on well-established models (reviewed in (Gutman and Nemeroff, 2002;Pryce and Feldon, 2003;Molet et al, 2014;Tractenberg et al, 2016)) and our prior work showing this MS protocol induces alterations in USV potentiation during an isolation-reunion protocol (Kaidbey et al, 2019). On P2, pups were weighed, litters culled to 8 pups (1:1 male-to-female ratio when possible), and randomly assigned to MS versus normally reared controls.…”

“…Frontal EcoG power was measured in MS versus control pups at postnatal days (P) 11-14 after a standard 3-hour daily MS protocol from P2 to P10. We evaluated EcoG during (1) naturally occurring behaviors such as arched back nursing and licking and grooming, (2) during behavioral transitions such as milk ejections and dam coming into nest, and (3) during an isolation-reunion paradigm we previously tested to induce pup ultrasonic potentiation following the same MS protocol (Kaidbey et al, 2019).…”

Altered environmental perception by parental stress and depression vulnerability: impact on mothers and offspring

“…The maternal separation paradigm (MS), used as a parental adverse event, is the most widely used animal model to study early life stress and disruptions of the infant-mother relationship 10 . Under MS, pups increase solicitation calls 11 , compelling mothers to increase their maternal behaviour as a response to pup needs 4 , which has been associated with increased oxytocin receptors (OXTR) expression 12 .…”