When presented with a light cue followed by food, some rats simply approach the foodcup (Nonorienters), while others first orient to the light in addition to displaying the food-cup approach behavior (Orienters). Cue-directed orienting may reflect enhanced attentional and/or emotional processing of the cue, suggesting divergent natures of cue-information processing in Orienters and Nonorienters. The current studies investigate how differences in cue processing might manifest in appetitive memory retrieval and updating using a paradigm developed to persistently attenuate fear responses (Retrieval-extinction paradigm; Monfils et al., 2009). First, we examined whether the retrieval-extinction paradigm could attenuate appetitive responses in Orienters and Nonorienters. Next, we investigated if the appetitive memory could be updated using reversal learning (fear conditioning) during the reconsolidation window (as opposed to repeated unreinforced trials, i.e., extinction). Both extinction and new fear learning given within the reconsolidation window were effective at persistently updating the initial appetitive memory in the Orienters, but not the Nonorienters. Since conditioned orienting is mediated by the amygdala central nucleus (CeA), our final experiment examined the CeA’s role in the retrieval-extinction process. Bilateral CeA lesions interfered with the retrieval-extinction paradigm—did not prevent spontaneous recovery of food-cup approach. Together, our studies demonstrate the critical role of conditioned orienting behavior and the CeA in updating appetitive memory during the reconsolidation window.

When a neutral cue is followed by a significant event such as food delivery, some animals become engaged with the cue itself and acquire cue-directed behaviors. One type of cue-directed behavior is observed following insertion of a lever used as a conditioned stimulus (CS). Rats showing robust approach behavior to the lever also display impulsivity and altered attention, as compared to rats showing behavior directed toward the reward delivery location. The current study used a light CS to categorize rats' propensity for cue-directed behavior, and assessed whether individual differences in impulsivity and related behaviors still emerged. During the light-food pairings, some rats displayed enhanced rearing or orienting to the light (Orienters) prior to showing food cup approach behavior, while other rats only showed food cup approach behavior (Nonorienters). Our results showed that Orienters made more impulsive and risky decisions in two different choice tasks, and were quicker to leave a familiar dark environment to enter a novel bright field. Orienters also showed less accurate target detection when a visual distractor was introduced during an attentional challenge. Our current study suggests that light CS-induced rearing/orienting behavior might not necessarily share an identical mechanism with lever CS-approach behavior in predicting impulsivity-related behaviors.

Individual differences in appetitive learning have long been reported, and generally divide into two classes of responses: cue- vs. reward-directed. The influence of cue- vs. reward-directed phenotypes on aversive cue processing, is less well understood. In the current study, we first categorized rats based on their predominant cue-directed orienting responses during appetitive Pavlovian conditioning. Then, we investigated the effect of phenotype on the latency to exit a familiar dark environment and enter an unfamiliar illuminated open field. Next, we examined whether the two phenotypes responded differently to a reconsolidation updating manipulation (retrieval+extinction) after fear conditioning. We report that the rats with a cue-directed (“orienting”) phenotype differentially respond to the open field, and also to fear conditioning, depending on US-intensity. In addition, our findings suggest that, regardless of appetitive phenotype or shock intensity, extinction within the reconsolidation window prevents spontaneous recovery of fear.

Conditioned orienting response (OR) is a form of cue-directed behavior thought to indicate increased attentional and/or motivational processing of reward-associated stimuli. OR as a phenotype has been shown to predict both direct drug proclivity in female rats and behaviors indirectly related to drug proclivity in male rats, but no extant research has compared males and females in terms of their OR behavior or its notable substrates. As females are at increased risk for substance abuse, and the ovarian hormone estradiol is often cited as a driving factor for this predilection, it is important to characterize sex differences between males and females and explore what, if any, contribution estradiol has in behaviors which predict substance abuse. In these experiments, male and female rats [intact or ovariectomized (OVX) with/without estradiol replacement] were compared on a battery of behavioral tasks, including OR, novelty-seeking, attentional set-shifting, and ultrasonic vocalizations (USVs) to amphetamine treatment. Female rats, regardless of estradiol replacement, had higher OR scores than males. OR score was a predictor of attention impairments, and estradiol availability contributed to this relationship in females. Sex differences were not observed in novelty-seeking, attentional set-shifting, or USV response to amphetamine; however, estradiol replacement did alter the presentation of these behaviors.

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