The social transmission of associative fear in rats : mechanisms and applications of fear conditioning by proxy
Pairing a neutral cue (e.g., a tone) with an inherently aversive unconditioned stimulus (US; e.g., a foot-shock) leads to future presentations of the now conditioned stimulus (CS) alone eliciting a conditioned response (e.g., freezing). This direct associative learning is only one technique under which individuals can learn about potential threats, but its convenient design and the robust production of responses makes direct fear conditioning the most frequently used paradigm in the research of fear and anxiety disorders. Fear can also be acquired from a social context, such as through observing the fear expression of a conspecific (Mineka et al., 1984, Mineka and Cook, 1993, Olsson et al., 2007, Olsson and Phelps, 2007). Utilizing a modified demonstrator-observer paradigm (fear conditioning by proxy) that allows for free interaction between subjects (see Bruchey et al., 2010; Jones et al., 2014), I explore the ability of rats to learn an associative fear response vicariously. In the experiments presented here, I (i) investigate the subject traits that bias rats to engage a social learning strategy; (ii) examine the neural mechanisms involved in this form of observational learning; and (iii) demonstrate how this paradigm can be incorporated into translationally-relevant tests of long term behavioral deficits resulting from early life trauma, in line with the health goals of the fear learning field in general (e.g., fear reduction). My results indicate that the identity of demonstrator animals as well as prior experience of the observer contributes to the expression of fear acquired vicariously. Additionally, I show that the social behaviors of caged rats are indicators of a social dominance hierarchy and are predictors of the potency of social fear transmission. This method of fear learning conserves some of the pathways necessary for direct fear learning (e.g., lateral amygdala) but is unique in that it requires regions necessary for executive control (e.g., anterior cingulate cortex) making the fear conditioning by proxy paradigm a novel tool for evaluating learning and behavior in the laboratory setting.