Excitatory second-order conditioning using a backward first-order conditioned stimulus: A challenge for prediction error reduction

Abstract

Prével and colleagues reported excitatory learning with a backward conditioned stimulus (CS) in a conditioned reinforcement preparation. Their results add to existing evidence of backward CSs sometimes being excitatory and were viewed as challenging the view that learning is driven by prediction error reduction, which assumes that only predictive (i.e., forward) relationships are learned. The results instead were consistent with the assumptions of both Miller's Temporal Coding Hypothesis and Wagner's Sometimes Opponent Processes (SOP) model. The present experiment extended the conditioned reinforcement preparation developed by Prével et al. to a backward second-order conditioning preparation, with the aim of discriminating between these two accounts. We tested whether a second-order CS can serve as an effective conditioned reinforcer, even when the first-order CS with which it was paired is a backward CS that elicits no responding. Evidence of conditioned reinforcement was found, despite no conditioned response (CR) being elicited by the first-order backward CS. The evidence of second-order conditioning in the absence of excitatory conditioning to the first-order CS is interpreted as a challenge to SOP. In contrast, the present results are consistent with the Temporal Coding Hypothesis and constitute a conceptual replication in humans of previous reports of excitatory second-order conditioning in rodents with a backward CS. The proposal is made that learning is driven by "discrepancy" with prior experience as opposed to " prediction error."

Higher-Order Conditioning With Simultaneous and Backward Conditioned Stimulus: Implications for Models of Pavlovian Conditioning

“…Parallel to these investigations, Barnet et al (1997) demonstrated that a backward CS1 can support stronger second-order conditioning compared to a forward first-order CS1, despite a lower CR to that backward stimulus. More recent observations by Prével et al (2019) are consistent with these findings. Specifically, the authors demonstrated that a second-order stimulus CS2 can function as an efficient conditioned reinforcer for instrumental response in the test phase, even when that stimulus was paired with a backward CS1 that did not evoke CR during phase 2.…”

“…Traditionally, investigations on higher-order conditioning involve forward CS2 → CS1 and CS1 → US pairings. However, far less investigated are procedures involving simultaneous or backward pairings (e.g., Prével et al, 2019 ). In this mini-review, we will argue that these procedures are actually particularly relevant for the understanding of Pavlovian conditioning.…”

Bed nucleus of the stria terminalis regulates fear to unpredictable threat signals

“…Specifically, we arranged a brief (10 s) auditory CS to either precede (forward conditioning, FW) or follow (backward conditioning, BW) a footshock US in rats. Although extensively-trained BW CSs become conditioned inhibitors that dampen responding to other first-order excitatory cues (Andreatta et al, 2012; Ayres et al, 1976; Christianson et al, 2011; Gerber et al, 2014; Moscovitch and LoLordo, 1968; Siegel and Domjan, 1971), minimally-trained BW CSs elicit excitatory conditioned responses that transfer across contexts (Ayres et al, 1987; Barnet and Miller, 1996; Bevins and Ayres, 1992; Chang et al, 2003; Connor et al, 2017; Heth, 1976; Mahoney and Ayres, 1976; Prével et al, 2018; Prével et al, 2016; Rescorla, 1968). After conditioning, we examined the effect of pharmacological inactivation of the BNST on freezing to FW or BW CSs.…”

Learning in reverse: Dopamine errors drive excitatory and inhibitory components of backward conditioning in an outcome-specific manner

“…Backward conditioning-when a reward is followed by a cue (rewardcue)-breaks this temporal mold and provides a serious challenge to current computational hypotheses of dopamine function. Backward conditioning can result in both excitatory and inhibitory associations [34][35][36][37][38] . That is, a backward cue is capable of exciting or inhibiting representation of associated rewards, which motivates the animal towards or away from that specific reward.…”