Appetitive context conditioning proactively, but transiently, interferes with expression of counterconditioned context fear

Abstract

Four experiments used rats to study appetitive-aversive transfer. Rats trained to eat a palatable food in a distinctive context and shocked in that context ate and did not freeze when tested 1 d later but froze and did not eat when tested 14 d later. These results were associatively mediated (Experiments 1 and 2), observed when rats were or were not food deprived (Experiments 1 and 2), and were not due to latent inhibition (Experiment 3). In contrast, rats trained to eat in the context and shocked there 13 d later froze and did not eat when tested 1 d after the shocked exposure. However, rats that received an additional eating session in the context 1 d before the shocked exposure ate and did not freeze when tested 1 d after the shocked exposure (Experiment 4). The results show that appetitive conditioning transiently interferes with aversive conditioning. They are discussed in terms of a weak context-shock association becoming stronger with the lapse of time (so-called fear incubation) or of the interference by the context -food association becoming weaker with the lapse of time.Pavlovian conditioning imbues neutral stimuli with emotional and/or motivational significance. A relatively innocuous stimulus paired with an aversive shock unconditioned stimulus (US) becomes a conditioned stimulus (CS), eliciting protective reflexes and defensive responses. That CS also suppresses appetitive activity (e.g., Estes and Skinner 1941), punishes contingent instrumental responses (e.g., Azrin 1960; for review, see Azrin and Holz 1966), and increases avoidance responses (e.g., Rescorla and LoLordo 1965; for review, see Rescorla and Solomon 1967). In contrast, a CS paired with an attractive food US elicits consummatory reflexes and approach responses, suppresses defensive responses (e.g., Grossen et al. 1969;Overmier and Bull 1970;Overmier et al. 1971), reinforces contingent instrumental responses (for review, see Wike 1966;Hendry 1969;Fantino 1977), and can increase responding in Pavlovian-Instrumental tasks (e.g., Estes 1948; for review, see Holmes et al. 2010). Such results have led to opponent-process theories of motivation (e.g., Konorski 1967;Bindra 1974;Gray 1975;Dickinson and Dearing 1979;Toates 1986). These theories differ in several respects but share the view that aversive and appetitive CSs excite contrasting central motivational states or systems and that excitation of one depresses activity in the other (for review, see Dickinson and Pearce 1977).An implication of these theories is that the development of defensive responses across pairings of an appetitive CS and an aversive US will be impaired, as will approach responses across pairings of an aversive CS and an appetitive US. This impairment will occur because the motivational information originally encoded by the CS is the opposite of that appropriate to the new US. Consistent with this implication, the development of approach responses is impaired across pairings of an aversive CS and an appetitive US (e.g., Peck and Bouton 1990), as is the development of wi...

Paraventricular Thalamus Controls Behavior during Motivational Conflict

“…Rats were tested twice, once in the aversive context and once in the appetitive context. As expected McNally, 2012, 2013;Holmes and Westbrook, 2014), rats expressed appetitive (i.e., magazine entries) and aversive (i.e., freezing) behavior in both contexts (Fig. 1E).…”

“…Here we studied motivational conflict using Pavlovian counterconditioning (Dickinson and Pearce, 1977;Lovibond and Dickinson, 1982;McNally, 2012, 2013;Holmes and Westbrook, 2014). In counterconditioning, a conditioned stimulus (CS) from one motivational class is transformed into a CS of a contrasting motivational class (e.g., signal for reward is transformed into a signal for danger).…”

Activation of D1/5 Dopamine Receptors: A Common Mechanism for Enhancing Extinction of Fear and Reward-Seeking Behaviors

“…There are many possibilities for this, including consolidation of the prediction error that occurred in extinction (Abraham et al, 2014), a D1-mediated prolonged window of inhibitory memory activity (Wagner, 1981), or counterconditioning of aversive fear memory by the rewarding properties of SKF81297 (Holmes and Westbrook, 2014). Our findings that SKF81297 induced a CPP when it was used as the US suggest that counterconditioning is a possibility for the enhanced fear extinction effects, and previous studies have shown that fear learning is subject to opponent interactions between appetitive and aversive processes (Nasser and McNally, 2012).…”

An arbiter model of motivational selection

“…However, this dominance is hardly universal. Other motivational states can trump fear (Burnett et al, 2016;Choi et al, 2019;Choi and McNally, 2017;Holmes and Westbrook, 2014). At some point, the hungry animal is willing to tolerate and then overcome adversity and fear to meet its metabolic need (Burnett et al, 2019;Burnett et al, 2016;Choi et al, 2019;Choi and McNally, 2017;Miller, 1960) just as a sick parent interrupts its own recuperation to care for its young (Aubert, 1999).…”