Ecologically relevant neurobehavioral assessment of the development of threat learning

Abstract

As altricial infants gradually transition to adults, their proximate environment changes. In three short weeks, pups transition from a small world with the caregiver and siblings to a complex milieu rich in dangers as their environment expands. Such contrasting environments require different learning abilities and lead to distinct responses throughout development. Here, we will review some of the learned fear conditioned responses to threats in rats during their ontogeny, including behavioral and physiological measures that permit the assessment of learning and its supporting neurobiology from infancy through adulthood. In adulthood, odor-shock conditioning produces robust fear learning to the odor that depends upon the amygdala and related circuitry. Paradoxically, this conditioning in young pups fails to support fear learning and supports approach learning to the odor previously paired with shock. This approach learning is mediated by the infant attachment network that does not include the amygdala. During the age range when pups transition from the infant to the adult circuit (10 -15 d old), pups have access to both networks: odor -shock conditioning in maternal presence uses the attachment circuit but the adult amygdala-dependent circuit when alone. However, throughout development (as young as 5 d old) the attachment associated learning can be overridden and amygdala-dependent fear learning supported, if the mother expresses fear in the presence of the pup. This social modulation of the fear permits the expression of defense reactions in life threatening situations informed by the caregiver but prevents the learning of the caregiver itself as a threat.

Amplitude modulation pattern of rat distress vocalisations during fear conditioning

“…To test this idea, in this article, we searched for AMs in an existing dataset of USVs emitted during a Pavlovian fear conditioning experiment 20 , 21 , in which an aversive unconditioned stimulus (US = foot-shock) was presented following a neutral conditioned stimulus (CS = peppermint odour cue). Fear conditioning is widely used in studies of memory and associative learning 22 – 25 . The strength of the fear memory is commonly assessed using overt behaviour analysis, such as freezing responses.…”

Sniffing response to an odor through development in rats: modulatory role of repetition and association with an aversive event

“…Odor fear conditioning has been well characterized during ontogeny and this literature has shown that fear learning emerges in rat pups around PN10 and is caused by the recruitment of the amygdala during the odor–shock conditioning (Sullivan et al 2000a; Moriceau et al 2006; Raineki et al 2009; Boulanger-Bertolus et al, 2016).…”

Ultrasonic Vocalizations Emission across Development in Rats: Coordination with Respiration and Impact on Brain Neural Dynamics

“…It is important to point out that while we described important differences in the emission of USV between infancy and adulthood, the consequences of USV emission on the infant brain remains entirely unknown at this point. Aversive events that induce USV have drastically different consequences at these two stages of development, and their memories also differentially affected the animal’s subsequent behavior [ 159 , 160 ]. The 22-kHz rat vocalizations present an evolutionary counterpart to human crying [ 161 ], and human infant crying and rat pup USV have been suggested to share some similarities [ 72 ].…”