Abstract
Early life adversity increases anxiety in adult rodents and primates, and increases the risk for developing post-traumatic disorder (PTSD) in humans. We hypothesized that early adversity impairs the use of learning signals -negative, aversive prediction errors–to reduce fear in uncertainty. To test this hypothesis, we gave adolescent rats a battery of adverse experiences then assessed adult performance in probabilistic Pavlovian fear conditioning and fear extinction. Rats were confronted with three cues associated with different probabilities of foot shock: one cue never predicted shock, another cue predicted shock with uncertainty, and a final cue always predicted shock. Control rats initially acquired fear to all cues, but rapidly reduced fear to the non-predictive and uncertain cues. Early adversity rats were slower to reduce fear to the non-predictive cue and never fully reduced fear to the uncertain cue. In extinction, all cues were presented in the absence of shock. Fear to the uncertain cue in discrimination, but not early adversity itself, predicted the reduction of fear in extinction. These results demonstrate early adversity impairs the use of negative aversive prediction errors to reduce fear, especially in situations of uncertainty.
Highlights
Probabilistic reinforcement in Pavlovian fear conditioning is a straightforward setting in which aversive prediction errors (APEs) contribute to fear reduction
Body Weight All rats had free access to water and food from the day they arrived until they began the Pavlovian fear conditioning procedure
We gave adolescent rats a battery of early adverse experiences and allowed them to mature without interruption
Summary
Adversity increases anxiety in adult rodents (Avital and Richter-Levin, 2005; Pohl et al, 2007; Tsoory et al, 2007; Franklin et al, 2010) and primates (Sánchez et al, 2005; Sanchez, 2006), and increases the risk for post-traumatic stress disorder (PTSD) in humans (Kessler et al, 1997; Breslau et al, 1999; Cloitre et al, 2009; Xie et al, 2010). Risk for acquiring PTSD increases as more types of adversity are experienced (Breslau et al, 1999; Xie et al, 2012). Increased anxiety in adverse-experienced individuals, such as those with PTSD, may partially result from an inability to effectively utilize aversive prediction errors (APEs) to reduce fear. APEs are learning signals generated by a discrepancy between actual and predicted aversive outcomes and come in two varieties: “positive” and “negative”. “Positive” and “negative” do not refer to the value of the outcome, but rather to the direction of the discrepancy. Probabilistic reinforcement in Pavlovian fear conditioning is a straightforward setting in which APEs contribute to fear reduction
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