Acquisition and extinction of conditioned suppression under two training procedures

Eight male albino rats acquired conditioned suppression under either predictable (Estes & Skinner, 1941) or random (Rescorla, 1968) procedures. The random procedure led to more generalized suppression (non-CS suppression) and greater resistance to extinction. In addition, the pattern of responding during the CS differed: the predictable group produced negatively accelerated cumulative records during early extinction trials; the random group produced positively accelerated cumulative records.     

Enhancement of food-rewarded instrumental responding by an appetitive conditioned stimulus

Four experiments are reported in which a stimulus (with a minimum duration of 60 s) signalling the delivery of “free” food was presented to rats lever-pressing for food available on a variable interval schedule. It was found that responding was enhanced in the presence of the stimulus when the baseline schedule of reinforcement was lean (Experiment I) and that the enhancement was dependent upon the pairing of the stimulus with free food (Experiments II and III). Experiment IV showed that an enhancement could be found after initial training in which stimulus-food pairings were given to subjects that were not concurrently lever pressing for food. It is argued that these results are consistent with the suggestion that an appetitive conditioned stimulus can energise appetitive instrumental behaviour.     

Extinction of goal tracking also eliminates the conditioned reinforcing effects of an appetitive conditioned stimulus

Previous studies have suggested that the effects of extinction are response-specific. The present study investigated whether an extinction treatment that eliminated goal tracking elicited by an appetitive conditioned stimulus (CS) would also eliminate the conditioned reinforcing effects of that CS. Rats were first trained on a goal-tracking procedure in which an auditory CS was paired with a food unconditioned stimulus. Animals learned to approach the location where the food was delivered. In a subsequent phase, rats in one group received extinction training that eliminated the goal-tracking elicited by the CS. Rats in the other group did not experience extinction of the food-paired CS. Then, both groups received a test for conditioned reinforcement in which leverpresses resulted in the brief presentation of the stimulus previously paired with food. This stimulus did not act as a conditioned reinforcer in the group that had been subjected to extinction training, but did serve as a conditioned reinforcer in the group that did not experience extinction. These results indicate that the effects of extinction generalize from the approach-eliciting to the conditioned reinforcing effects of an appetitive CS.     

Counteraction between two kinds of conditioned inhibition training

In a Pavlovian fear-conditioning preparation, we investigated the effects of combining Pavlovian and explicitly unpaired inhibition treatments. A summation test for inhibition suggested a strong tendency toward unpaired inhibition when that treatment was administered alone and found robust Pavlovian inhibition when that treatment was administered alone, but detected little behavior indicative of inhibition in subjects that experienced both treatments during training. The retardation test showed reliable unpaired and Pavlovian inhibition when these treatments were administered alone but no indication of inhibition in subjects that experienced both treatments. These counterintuitive results suggest that in some circumstances the effects of two inhibitory treatments are not additive but rather counteractive. The present results provide some information about the nature of conditioned inhibition and, more generally, cue interaction.     

Amnesia produced by anisomycin in an appetitive task is not due to conditioned aversion

Two experiments investigated the effects of lithium chloride (LiCl) and anisomycin (ANI) in a water reward Y-maze task. In Experiment 1, male CD-1 mice given weak or strong training were injected post-training with either saline or LiCl (150 mg/kg), which has been reported to produce conditioned aversion in mice. One day after training, both LiCl groups avoided the rewarded arm of the maze and drank less water than saline-injected controls. Two days after training, the strongly trained LiCl mice showed avoidance, while both LiCl groups drank less water. In Experiment 2, weakly trained mice given pre- and post-training ANI (30 mg/kg) were amnesic on the second test day compared to mice that received post-trial saline. However, water consumption was increased on the test day for both groups. LiCl produced a different pattern of results than ANI in this task. On the basis of these results, it is suggested that amnesia produced by ANI is due to impaired memory formation and not to conditioned aversion.     

A change of context can enhance performance of an aversive but not of an appetitive conditioned response

In four experiments rats received pairings of one auditory CS and mild shock in one context and of a second auditory CS and shock in a second context. When tested with one of these CSs in the context in which it had never been experienced, they consistently showed enhanced levels of suppression. In one of these experiments, suppression was measured over 15-sec intervals throughout a 90-sec long CS. A change of context resulted in an increased level of suppression at all points throughout the CS, a finding which does not encourage the belief that it was due to an increase in unconditioned suppression at the onset of the CS. Another experiment provided equally little support for an alternative account in terms of increased arousal. The results therefore suggest that a change of context can increase the level of conditioned suppression elicited by a CS paired with mild shock. Two final experiments employing the same CSs and contexts, however, found no evidence that a change of context had any effect at all on the performance of an appetitively conditioned response.     

Signaling and affective functions of conditioned aversive stimuli in an appetitive choice discrimination: US intensity effects

Different groups of rats received Pavlovian aversive conditioning in which US-shock intensity (0.25–1.0 mA) and CS-US correlation (+, 0, ?) were factorially varied. Then, the CS was administered for each group contingent upon the reinforced response in an appetitive choice discrimination. Absolute and ratio measures of speed of running in the presence of the CS showed that, at the start of discrimination training, CS+ suppressed and CS- facilitated performance. However, later in training but prior to any evidence of choice learning, these speed effects reversed, with the magnitude of both the initial and reversed effects being a positive function of US intensity. Consistent with the reversal of speeds, associative (choice) measures showed that CS+ facilitated and CS- retarded discrimination learning relative to CSo and, within limits, these effects were also amplified by stronger USs. The findings suggest that a CS has both affective (motivational) and signaling (associative) functions and that both are influenced by US intensity; however, the CS's affective property is rapidly extinguished in the presence of a hedonicly different reinforcer, while leaving the CS's signaling property largely intact. Hence, the CS functions as a transformed signal for the new (appetitive) reinforcer and facilitates or retards learning by mediating the reinforcer's presence (CS+) or absence (CS-).     

Stimulus factors in aversive controls: conditioned suppression after equal training to two stimuli

Pigeons trained to peck a key for food were periodically presented with tones ending with electrical shock until tone presentation consistently suppressed ongoing pecks. Shock was then discontinued and gradients of stimulus generalization were assessed by presenting tones with frequencies above, below, and at the frequencies of those used to develop conditioned suppression. When the training tones had frequencies at 670 and 1500 cps, resulting gradients were bi-modal with peak suppression at 670 and 1500 cps. Of the other test tones, 1000 cps produced the most suppression. When the training tones had frequencies at 450 and 2250 cps, bi-modal gradients were again obtained with peak suppression to the 450 and 2250 cps tones. Of the other test tones, 1000 cps produced the least suppression. These results support the hypothesis that generalized response tendencies summate.     

Extinction training regulates neuroadaptive responses to withdrawal from chronic cocaine self-administration

Cocaine produces multiple neuroadaptations with chronic repeated use. Many of these neuroadaptations can be reversed or normalized by extinction training during withdrawal from chronic cocaine self-administration in rats. This article reviews our past and present studies on extinction-induced modulation of the neuroadaptive response to chronic cocaine in the mesolimbic dopamine system, and the role of this modulation in addictive behavior in rats. Extinction training normalizes tyrosine hydroxylase levels in the nucleus accumbens (NAc) shell, an effect that could help ameliorate dysphoria and depression associated with withdrawal from chronic cocaine use. Extinction training also increases levels of GluR1 and GluR2/3 AMPA receptor subunits, while normalizing deficits in NR1 NMDA receptor subunits, in a manner consistent with long-term potentiation of excitatory synapses in the NAc shell. Our results suggest that extinction-induced increases in AMPA and NMDA receptors may restore deficits in cortico-accumbal neurotransmission in the NAc shell and facilitate inhibitory control over cocaine-seeking behavior. Other changes identified by gene expression profiling, including up-regulation in the AMPA receptor aggregating protein Narp, suggest that extinction training induces extensive synaptic reorganization. These studies highlight potential benefits for extinction training procedures in the treatment of drug addiction.     

Different responses of two strains of chickens to different training procedures for magnetic directions

In previous conditioning experiments training domestic chickens to magnetic directions, a brown strain solved the task, whereas a white strain seemed unable to do so (Freire et al. Anim Cogn 11:547–552, 2008). To test whether this was possibly caused by loss of magnetic compass orientation in the white chickens, we analyzed the distribution of cryptochrome 1a, the candidate receptor molecule mediating magnetic compass information, in the retinae of Lohmann Browns and White Leghorns and found no difference between the two strains. Yet, subsequent training experiments replicated the former findings: Lohmann Browns used the magnetic field to find an imprinting stimulus hidden behind the screen in a specific magnetic direction, whereas White Leghorns did not solve the task. However, when we altered the training method by training also in a magnetic field with North shifted to geographic East and including a punishment for incorrect choices, the performance of White Leghorns improved to a significant preference for the expected directions. The Lohmann Browns, on the other hand, seemed frightened and chose randomly. Our results thus demonstrate the crucial role of the training method for conditioning to magnetic stimuli, with differences found even between strains of the same species.     

Performance of pigeons on delayed simple and conditional discriminations under equivalent training procedures

A pair of experiments investigated the short-term memory of pigeons under delayed simple and conditional discriminations. Trial sequences in both discriminations consisted of a color as the sample stimulus, a memory interval, a line orientation as the test stimulus, and a trial outcome, which was either food reinforcement or blackout. Pecking rates during the test stimulus defined discrimination performance. In the simple discrimination, the sample provided the necessary information regarding the subsequent trial outcome. In the conditional discrimination, the sample and test stimuli conjointly provided this information. In Experiment 1, the two procedures were compared with independent groups of pigeons. In Experiment 2, the comparison was made within subjects. The simple discrimination was acquired more quickly and was performed better with a memory requirement. Introduction of long delays disrupted performance even at shorter delays in both discriminations. Postulation of prospective as well as retrospective mediating processes facilitates the interpretation of these results.     

Control of appetitive and aversive taste-reactivity responses by an auditory conditioned stimulus in a devaluation task: a FOS and behavioral analysis

Through associative learning, cues for biologically significant reinforcers such as food may gain access to mental representations of those reinforcers. Here, we used devaluation procedures, behavioral assessment of hedonic taste-reactivity responses, and measurement of immediate-early gene (IEG) expression to show that a cue for food engages behavior and brain activity related to sensory and hedonic processing of that food. Rats first received a tone paired with intraoral infusion of sucrose. Then, in the absence of the tone, the value of sucrose was reduced (Devalue group) by pairing sucrose with lithium chloride (LiCl), or maintained (Maintain group) by presenting sucrose and LiCl unpaired. Finally, taste-reactivity responses to the tone were assessed in the absence of sucrose. Devalue rats showed high levels of aversive responses and minimal appetitive responses, whereas Maintain rats exhibited substantial appetitive responding but little aversive responding. Control rats that had not received tone-sucrose pairings did not display either class of behaviors. Devalue rats showed greater FOS expression than Maintain rats in several brain regions implicated in devaluation task performance and the display of aversive responses, including the basolateral amygdala, orbitofrontal cortex, gustatory cortex (GC), and the posterior accumbens shell (ACBs), whereas the opposite pattern was found in the anterior ACBs. Both Devalue and Maintain rats showed greater FOS expression than control rats in amygdala central nucleus, GC, and both subregions of ACBs. Thus, through associative learning, auditory cues for food gained access to neural processing in several brain regions importantly involved in the processing of taste memory information.     

Reduction of contextual control of conditioned responses by extended Pavlovian training in an insect

The effect of repetitive training on learned behavior has been an important subject in neuroscience. In instrumental conditioning in mammals, learned action early in training is often goal-driven and controlled by outcome expectancy, but as training progresses, it becomes more habitual and insensitive to outcome devaluation. Similarly, we recently showed in Pavlovian conditioning in crickets (Gryllus bimaculatus) that a conditioned response (CR) is initially sensitive to devaluation of the unconditioned stimulus but becomes insensitive to it after extended training. It is known that habitual responses after extended instrumental training are characterized by a higher context specificity than are initial goal-directed actions in mammals. In this study, we investigated whether this is applicable to Pavlovian conditioning in crickets. In crickets that received a standard amount of training to associate an odor with water reward under illumination, CR under illumination was stronger than that in the dark. In crickets that received extended training under illumination, on the other hand, the level of CR did not differ in different light conditions. Further experiments confirmed that context specificity decreases with the development of behavioral automaticity by extended training, as opposed to findings in instrumental training in mammals. We conclude that the nature of habitual behaviors after extended training differs in different learning systems of animals.

In humans, habitual behavior often underlies dysfunctional behaviors such as drug addiction (Everitt et al. 2001) and obsessive-compulsive disorder (Gillan et al. 2011). It is for this reason that much research conducted on behavioral neuroscience and psychology has aimed to understand the effects of repetitive training on the performance of learned actions or, in other words, the development of habits (Gardner 2015; Wood and Rünger 2016). One of the most common findings in instrumental conditioning in mammals is that actions in an early stage of training are more goal-driven; i.e., they are controlled by the specific outcome (reinforcer) of their actions. However, as training proceeds, behaviors often become more automatic and independent of the actual value of the outcome, although both the goal-driven and habitual behavioral components often coexist in both early and later stages of training (Dickinson 1985; Yin and Knowlton 2006; Kosaki and Dickenson 2010; Smith and Graybiel 2014). Goal-directed actions and habitual behavior can be distinguished by using an outcome devaluation procedure in which the value of the outcome (reward) is reduced by aversive conditioning (Adams 1982; Dickinson 1985) or by outcome-specific satiation (Balleine and Dickinson 1998).We have investigated associative processes underlying Pavlovian conditioning and its possible neural substrates in the cricket Gryllus bimaculatus (Unoki et al. 2005; Mizunami et al. 2009; Mizunami and Matsumoto 2017; Mizunami et al. 2018), and we recently found that the conditioned response (CR) to an odor (conditioned stimulus, CS) diminishes when the value of water reward (unconditioned stimulus [US]) is reduced after satiation early in training but that it becomes insensitive to US devaluation after extended training in crickets (Mizunami et al. 2019). To our knowledge, these results provide the first evidence of increased automaticity of learned behavior by extended Pavlovian training in any animals. Crickets that received four-trial training to associate an odor CS with water US, which we refer to as standard training, exhibited no CR after water had been given until satiation before the test. On the other hand, crickets that received extended training (i.e., four conditioning trials per day on three consecutive days) exhibited the same level of CR regardless of whether they had been provided with water until satiation or not before the test.Notably, in instrumental conditioning in mammals, it has been documented that habitual behavior that is insensitive to outcome devaluation has features that are distinct from those of goal-directed behavior typically seen after limited training. The most notable one is its higher context specificity: Habitual responses are more likely to occur in the context in which training occurred than outside that context (in rats) (Thrailkill and Bouton 2015). Similarly, in humans, such context specificity is considered a hallmark of the habitual behavior formed by repetition of the same learned responses and it is considered a critical feature to which special attention must be paid in the therapy of mal-adaptive habits (Tricomi et al. 2009; Gardner 2015; Wood and Rünger 2016).The aim of this study was to determine whether the same context specificity that is observed in the habitual response after extended training in mammals is applicable to Pavlovian conditioning in insects. To do so, we performed standard or extended training for crickets under illumination, and their CRs were tested under illumination or in the dark. We used light and darkness as contexts since we observed that a change of background light level between training and testing influences the level of CRs in one paradigm of Pavlovian conditioning in crickets (Matsumoto and Mizunami 2004).     

A preliminary evaluation of two behavioral skills training procedures for teaching abduction-prevention skills to schoolchildren

Although child abduction is a low-rate event, it presents a serious threat to the safety of children. The victims of child abduction face the threat of physical and emotional injury, sexual abuse, and death. Previous research has shown that behavioral skills training (BST) is effective in teaching children abduction-prevention skills, although not all children learn the skills. This study compared BST only to BST with an added in situ training component to teach abduction-prevention skills in a small-group format to schoolchildren. Results showed that both programs were effective in teaching abduction-prevention skills. In addition, the scores for the group that received in situ training were significantly higher than scores for the group that received BST alone at the 3-month follow-up assessment.     

Reinstatement of fear to an extinguished conditioned stimulus: two roles for context

The authors studied the role of context in reinstatement. Freezing was reinstated when the conditioned stimulus (CS) was extinguished in 1 context and rats moved to another context for reexposure to the shock unconditioned stimulus (US) and test. It was also reinstated (rather than renewed) when rats were shocked in the extinction context and moved to another context for test. This reinstatement was CS specific and reduced by nonreinforced exposures to the extinction context. Rats shocked in the context in which a stimulus had been preexposed froze when tested in another context. These findings suggest 2 roles for context in reinstatement: conditioning of the test context (M. E. Bouton, 1993) and mediated conditioning by the extinction context (P. C. Holland, 1990).