Using Pavlovian Higher-Order Conditioning Paradigms to Investigate the Neural Substrates of Emotional Learning and Memory

University of Minnesota, Minneapolis, Minnesota 55455, USA.
Learning & Memory (Impact Factor: 3.66). 09/2000; 7(5):257-66. DOI: 10.1101/lm.35200
Source: PubMed


In first-order Pavlovian conditioning, learning is acquired by pairing a conditioned stimulus (CS) with an intrinsically motivating unconditioned stimulus (US; e.g., food or shock). In higher-order Pavlovian conditioning (sensory preconditioning and second-order conditioning), the CS is paired with a stimulus that has motivational value that is acquired rather than intrinsic. This review describes some of the ways higher-order conditioning paradigms can be used to elucidate substrates of learning and memory, primarily focusing on fear conditioning. First-order conditioning, second-order conditioning, and sensory preconditioning allow for the controlled demonstration of three distinct forms of memory, the neural substrates of which can thus be analyzed. Higher-order conditioning phenomena allow one to distinguish more precisely between processes involved in transmission of sensory or motor information and processes involved in the plasticity underlying learning. Finally, higher-order conditioning paradigms may also allow one to distinguish between processes involved in behavioral expression of memory retrieval versus processes involved in memory retrieval itself.

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    • "As noted earlier, Pavlovian higher order stimulus control (Holland & Rescorla, 1975; Rizely & Rescola, 1972) is not evident beyond second-order conditioning (Gewirtz & Davis, 2000), whereas operant chains have numerous links coupled by multiple discriminative stimuli (Lattal & Crawford-Godbey, 1985). Thus, distal S D s in long heterogeneous operant chains are not likely to evoke respondents; however, they can set the occasion for the more proximal response and also maintain the response for which they are consequential. "
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    ABSTRACT: Drug abuse remains costly. Drug-related cues can evoke cue-reactivity and craving, contributing to relapse. The Pavlovian extinction-based cue-exposure therapy (CET) has not been very successful in treating drug abuse. A functional operant analysis of complex rituals involved in CET is outlined and reinterpreted as an operant heterogeneous chain maintained by observing responses, conditioned reinforcers, and discriminative stimuli. It is further noted that operant functions are not predicated on Pavlovian processes but can be influenced by them in contributing to relapse; several empirical studies from the animal and human literature highlight this view. Cue-reactivity evoked by Pavlovian processes is conceptualized as an operant establishing/motivating operation. CET may be more effective in incorporating an operant-based approach that takes into account the complexity of Pavlovian-operant interaction. Extinction of the operant chain coupled with the shaping of alternative behaviors is proposed as an integrated therapy. It is proposed that operant-based drug abuse treatments (contingency management, voucher programs, and the therapeutic work environment) might consider incorporating cue-reactivity, as establishing/motivating operations, to increase long-term success-a hybrid approach based on Pavlovian-operant interaction.
    Full-text · Article · Sep 2013 · The Psychological record
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    • "The present findings suggest that sensory preconditioning in rabbit pups is not based on the associative chain CS2 CS1 response but rather on a direct link CS2 response. This seems in contradiction with studies suggesting that sensory preconditioning is based on stimulus–stimulus association in adult rodents (for reviews, see Gewirtz and Davis 2000; Parkes and Westbrook 2011). For instance , extinction of the first-order CS1 in adult rats eliminated CS2 responding in sensory preconditioning (Rizley and Rescorla 1972). "
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    ABSTRACT: This study evaluated whether olfactory preconditioning is functional in newborn rabbits and based on joined or independent memory of odorants. First, after exposure to odorants A+B, the conditioning of A led to high responsiveness to odorant B. Second, responsiveness to B persisted after amnesia of A. Third, preconditioning was also functional with two overlapping pairs of odorants (A+B and B+C) and amnesia of one odorant did not affect memory of the others. Thus, incidental pairing of odorants allows reinforcement of one odorant to implicitly reinforce the others, the bond then vanishes, and the memory of each element becomes independent.
    Full-text · Article · Aug 2013 · Learning & memory (Cold Spring Harbor, N.Y.)
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    • "Therefore, the main aim of the current study was to assess the effects of certain procedural variables on the impaired extinction phenotype of the S1 mouse strain and, by comparison, the good extinguishing B6 mouse strain. The specific variables we studied were 1) the interval between conditioning and extinction [23-25], 2) the interval between cues during extinction training [26-28], 3) single-cue exposure before extinction training [29-32], and 4) extinction of a second-order conditioned cue [33,34]. "
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    ABSTRACT: Various neuropsychiatric conditions, including posttraumatic stress disorder (PTSD), are characterized by deficient fear extinction, but individuals differ greatly in risk for these. While there is growing evidence that fear extinction is influenced by certain procedural variables, it is unclear how these influences might vary across individuals and subpopulations. To model individual differences in fear extinction, prior studies identified a strain of inbred mouse, 129S1/SvImJ (S1), which exhibits a profound deficit in fear extinction, as compared to other inbred strains, such as C57BL/6 J (B6). Here, we assessed the effects of procedural variables on the impaired extinction phenotype of the S1 strain and, by comparison, the extinction-intact B6 strain. The variables studied were 1) the interval between conditioning and extinction, 2) the interval between cues during extinction training, 3) single-cue exposure before extinction training, and 4) extinction of a second-order conditioned cue. Conducting extinction training soon after ('immediately') conditioning attenuated fear retrieval in S1 mice and impaired extinction in B6 mice. Spacing cue presentations with long inter-trial intervals during extinction training augmented fear in S1 and B6 mice. The effect of spacing was lost with one-trial fear conditioning in B6, but not S1 mice. A single exposure to a conditioned cue before extinction training did not alter extinction retrieval, either in B6 or S1 mice. Both the S1 and B6 strains exhibited robust second-order fear conditioning, in which a cue associated with footshock was sufficient to serve as a conditioned exciter to condition a fear association to a second cue. B6 mice extinguished the fear response to the second-order conditioned cue, but S1 mice failed to do so. These data provide further evidence that fear extinction is strongly influenced by multiple procedural variables and is so in a highly strain-dependent manner. This suggests that the efficacy of extinction-based behavioral interventions, such as exposure therapy, for trauma-related anxiety disorders will be determined by the procedural parameters employed and the degree to which the patient can extinguish.
    Full-text · Article · Jul 2013 · Biology of Mood and Anxiety Disorders
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