Variation in the effectiveness of reinforcement and nonreinforcement in generating different conditioned behaviors.

Rat autoshaping procedures generate two readily measurable conditioned responses: During lever presentations that have previously signaled food, rats approach the food well (called goal-tracking) and interact with the lever itself (called sign-tracking). We investigated how reinforced and nonreinforced trials affect the overall and temporal distributions of these two responses across 10-second lever presentations. In two experiments, reinforced trials generated more goal-tracking than sign-tracking, and nonreinforced trials resulted in a larger reduction in goal-tracking than sign-tracking. The effect of reinforced trials was evident as an increase in goal-tracking and reduction in sign-tracking across the duration of the lever presentations, and nonreinforced trials resulted in this pattern transiently reversing and then becoming less evident with further training. These dissociations are consistent with a recent elaboration of the Rescorla-Wagner model, HeiDI (Honey, R.C., Dwyer, D.M., & Iliescu, A.F. (2020a). HeiDI: A model for Pavlovian learning and performance with reciprocal associations. Psychological Review, 127, 829-852.), a model in which responses related to the nature of the unconditioned stimulus (e.g., goal-tracking) have a different origin than those related to the nature of the conditioned stimulus (e.g., sign-tracking).

Placental endocrine insufficiency programs anxiety, deficits in cognition and atypical social behaviour in offspring.

Abnormally elevated expression of the imprinted PHLDA2 gene has been reported in the placenta of human babies that are growth restricted in utero in several studies. We previously modelled this gene alteration in mice and found that just 2-fold increased expression of Phlda2 resulted in placental endocrine insufficiency. In addition, elevated Phlda2 was found to drive fetal growth restriction (FGR) of transgenic offspring and impaired maternal care by their wildtype mothers. Being born small and being exposed to suboptimal maternal care have both been associated with the increased risk of mental health disorders in human populations. In the current study we probed behavioural consequences of elevated Phlda2 for the offspring. We discovered increased anxiety-like behaviours, deficits in cognition and atypical social behaviours, with the greatest impact on male offspring. Subsequent analysis revealed alterations in the transcriptome of the adult offspring hippocampus, hypothalamus and amygdala, regions consistent with these behavioural observations. The inclusion of a group of fully wildtype controls raised in a normal maternal environment allowed us to attribute behavioural and molecular alterations to the adverse maternal environment induced by placental endocrine insufficiency rather than the specific gene change of elevated Phlda2. Our work demonstrates that a highly common alteration reported in human FGR is associated with negative behavioural outcomes later in life. Importantly, we also establish the experimental paradigm that placental endocrine insufficiency can program atypical behaviour in offspring highlighting the under-appreciated role of placental endocrine insufficiency in driving disorders of later life behaviour.

Fearfulness: An important addition to the starter kit for distinctively human minds.

Grossmann's impressive article indicates that - along with attentional biases, expansion of domain-general processes of learning and memory, and other temperamental tweaks - heightened fearfulness is part of the genetic starter kit for distinctively human minds. The learned matching account of emotional contagion explains how heightened fearfulness could have promoted the development of caring and cooperation in our species.

Associations and hallucinations in mice and men.

Powers et al. (2017, Science, 357(6351), 596-600) report that Pavlovian conditioning can result in the perception of a stimulus in its absence, and that this effect is related to hallucinations outside the laboratory. Considered alongside similar studies in animals, this suggests that associatively produced perceptual processing offers a means to study hallucination-like behaviour in the animal laboratory.

Calorie seeking, but not hedonic response, contributes to hyperphagia in a mouse model for Prader-Willi syndrome.

Prader-Willi syndrome (PWS) is a neurodevelopmental disorder caused by deletion or inactivation of paternally expressed imprinted genes on human chromosome 15q11-q13, the most recognised feature of which is hyperphagia. This is thought to arise as a consequence of abnormalities in both the physiological drive for food and the rewarding properties of food. Although a number of mouse models for PWS exist, the underlying variables dictating maladaptive feeding remain unknown. Here, feeding behaviour in a mouse model in which the imprinting centre (IC) of the syntenic PWS interval has been deleted (PWS(ICdel) mice) is characterised. It is demonstrated that PWS(ICdel) mice show hyperghrelinaemia and increased consumption of food both following overnight fasting and when made more palatable with sucrose. However, hyperphagia in PWS(ICdel) mice was not accompanied by any changes in reactivity to the hedonic properties of palatable food (sucrose or saccharin), as measured by lick-cluster size. Nevertheless, overall consumption by PWS(ICdel) mice for non-caloric saccharin in the licking test was significantly reduced. Combined with converging findings from a continuous reinforcement schedule, these data indicate that PWS(ICdel) mice show a marked heightened sensitivity to the calorific value of food. Overall, these data indicate that any impact of the rewarding properties of food on the hyperphagia seen in PWS(ICdel) mice is driven primarily by calorie content and is unlikely to involve hedonic processes. This has important implications for understanding the neural systems underlying the feeding phenotype of PWS and the contribution of imprinted genes to abnormal feeding behaviour more generally.

A critical role for the hippocampus and perirhinal cortex in perceptual learning of scenes and faces: complementary findings from amnesia and FMRI.

It is debated whether subregions within the medial temporal lobe (MTL), in particular the hippocampus (HC) and perirhinal cortex (PrC), play domain-sensitive roles in learning. In the present study, two patients with differing degrees of MTL damage were first exposed to pairs of highly similar scenes, faces, and dot patterns and then asked to make repeated same/different decisions to preexposed and nonexposed (novel) pairs from the three categories (Experiment 1). We measured whether patients would show a benefit of prior exposure (preexposed > nonexposed) and whether repetition of nonexposed (and preexposed) pairs at test would benefit discrimination accuracy. Although selective HC damage impaired learning of scenes, but not faces and dot patterns, broader MTL damage involving the HC and PrC compromised discrimination learning of scenes and faces but left dot pattern learning unaffected. In Experiment 2, a similar task was run in healthy young participants in the MRI scanner. Functional region-of-interest analyses revealed that posterior HC and posterior parahippocampal gyrus showed greater activity during scene pattern learning, but not face and dot pattern learning, whereas PrC, anterior HC, and posterior fusiform gyrus were recruited during discrimination learning for faces, but not scenes and dot pattern learning. Critically, activity in posterior HC and PrC, but not the other functional region-of-interest analyses, was modulated by accuracy (correct > incorrect within a preferred category). Therefore, both approaches revealed a key role for the HC and PrC in discrimination learning, which is consistent with representational accounts in which subregions in these MTL structures store complex spatial and object representations, respectively.

Microstructural analysis of negative anticipatory contrast: A reconsideration of the devaluation account.

An animal's appetitive behavior is not a fixed response to current stimulation but can be affected by the anticipation of future events. For example, rats regularly given access to a moderately valued solution followed by a higher value solution (e.g., 4 % sucrose → 32 % sucrose) consume less of the initial solution than in control conditions where the initial solution is not followed by a higher value solution (e.g., 4 % sucrose → 4 % sucrose). Previous analyses have suggested that this negative anticipatory contrast effect does not depend on the "expectation" of a valuable stimulus producing a functional devaluation of a currently available stimulus of lesser value. In a within-subjects anticipatory contrast procedure, this study revealed that both consumption and the mean size of licking clusters were smaller for a 4 % sucrose solution on days when it preceded 32 % sucrose than on days when 4 % preceded 4 %. Since lick cluster size typically bears a positive monotonic relationship with the concentration of palatable solutions, this reduction is indicative of a decrease in the palatability/hedonic value of the solution subject to contrast. As such, we provide direct evidence that negative anticipatory contrast does produce a functional devaluation of the solution, thus challenging prevailing theoretical assumptions.

Instrumental responses and Pavlovian stimuli as temporal referents in a peak procedure.

Three experiments investigated whether the nature of the temporal referent affects timing behaviour in rats. We used a peak procedure and assessed timing of food well activity as a function of whether the referent was an instrumental response (a lever press that resulted in the withdrawal of the lever) or a conditioned stimulus (CS) that was 2 s in Experiment 1, 500 ms in Experiment 2, and 800 ms in Experiment 3. In all experiments, the interval between the offset of the temporal referent and food was 5 s. The curve fits for each experiment revealed no differences in peak time, but magazine responding immediately following the CS was higher than following a lever press. This pattern of results was interpreted as reflecting a combination of (a) ambiguity in which component of the 500 ms-2-s auditory stimulus was serving as the referent and (b) response competition between lever pressing and magazine activity. Critically, these results suggest that peak timing in rats is unaffected by whether a lever press or CS serves as the referent. This conclusion is consistent with theoretical models of timing behaviour, but not with evidence from humans showing that the subjective perception of time is affected by whether the cause of an outcome was self-generated or not.

Prediction error in models of adaptive behavior.

Pavlovian conditioning is evident in every species in which it has been assessed, and there is a consensus about its interpretation across behavioral,1,2 brain,3,4,5,6 and computational analyses7,8,9,10,11: conditioned behavior reflects the formation of a directional associative link from the memory of one stimulus (e.g., a visual stimulus) to another (e.g., food), with learning stopping when there is no error between the prediction generated by the visual stimulus and what happens next (e.g., food). This consensus fails to anticipate the results that we report here. In our experiments with rats, we find that arranging predictive (visual stimulus→food) and nonpredictive (food→visual stimulus) relationships produces marked and sustained changes in conditioned behaviors when the visual stimulus is presented alone. Moreover, the type of relationship affects (1) the distribution of conditioned behaviors related to the properties of both food (called goal-tracking) and the visual stimulus (called sign-tracking) and (2) when in the visual stimulus, these two behaviors are evident. These results represent an impetus for a fundamental shift in how Pavlovian conditioning is interpreted: animals learn about the relationship between two stimuli irrespective of the order in which they are presented, but they exhibit this knowledge in different ways. This interpretation and our new results are captured by a recent model of Pavlovian conditioning,12,13 HeiDI, and both are consistent with the need for animals to represent the fact that the impact of a cause (e.g., the ingestion of nutrients or the bite of a predator) can be felt before or after the cause has been perceived.

Switching from sucrose to saccharin: Extended successive negative contrast is not maintained by hedonic changes.

Previous experiments found that acceptance of saccharin by rats was reduced if they had prior experience of sucrose or some other highly palatable solution. This reduction in saccharin consumption was particularly extended after a switch from sucrose. On the surface, this seems to correspond to a successive negative contrast (SNC) effect. This term was coined by C. F. Flaherty to describe the situation where consumption of a target solution is reduced by prior experience of a more valuable solution, typically a more concentrated version of the target solution. However, SNC effects are normally transient and assessed relative to a nonshifted control. Here, we confirm that the reduction in consumption seen when shifting from sucrose to saccharin is persistent and is seen relative to the traditional unshifted control. In addition, an analysis of licking microstructure showed that the shift from sucrose to saccharin suppressed the hedonic value of saccharin relative to controls, but this effect was less persistent than consumption suppression. Interestingly, a similar dissociation is observed in extinction of conditioned taste aversion (CTA): suppression of consumption produced by CTA is far more persistent than suppression of hedonic value. The comparison of results across procedures suggests that persistent SNC produced by a qualitative downshift from sucrose to saccharin appears different from quantitative downshifts in the concentration of a single solution, and qualitative downshift effects may involve CTA. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Odor-taste pairings lead to the acquisition of negative hedonic qualities by the odor in aversion learning.

Three experiments examined the affective responses conditioned to an odorous stimulus in the taste-mediated odor aversion learning paradigm. Experiment 1 analyzed the microstructure of licking behavior during voluntary consumption. Before conditioning, water-deprived rats had access to a bottle containing either a tasteless odor (0.01% amyl acetate) diluted in water or mixed with 0.05% saccharin. Next, the rats were injected with either LiCl or saline immediately after drinking saccharin. At test, they received the odor and taste solutions on separate days. Lick cluster size was used as a direct measure of the hedonic response to the odor cue. Rats receiving odor-taste pairings prior to the saccharin devaluation showed both lower consumption and lick cluster size, reflecting a reduced hedonic evaluation of the odor. Experiments 2a and 2b used the orofacial reactivity method. After pretraining in the drinking boxes with the odor alone or mixed with saccharin, the rats were intraorally infused with saccharin before injection with LiCl or saline. At test, they were infused in separate sessions with the odor and taste and their orofacial reactions video recorded. There were increased aversive orofacial responses to the odor in rats that had prior odor-taste experience, a result indicating a negative hedonic evaluation of the odor. These results provide evidence of conditioned changes in affective value of odor cues through taste-mediated learning and are consistent with the idea that odor-taste pairings lead to the acquisition of taste qualities by the odor.

An evaluation of hedonic responses in taste-potentiated odor aversion using the analysis of licking microstructure and orofacial reactivity.

Two experiments examined the hedonic responses conditioned to odor cues in the phenomenon of taste-potentiated odor aversion. Experiment 1 analyzed the microstructure of licking behavior during voluntary consumption. A tasteless odor (amyl acetate) was delivered to rats either diluted in water or mixed with saccharin before being injected with LiCl. At test, subjects which had received the odor-taste compound during conditioning showed both lower odor consumption and lick cluster size, a result indicating an increased negative evaluation of the odor. Experiment 2 examined the orofacial reactions elicited by the odor as index of its hedonic impact. During conditioning, the rats were intraorally infused with either the odor alone or the odor-saccharin compound before being injected with LiCl. At test, they were infused with the odor and their orofacial responses video recorded. More aversive orofacial responses were elicited by the odor cue in rats that had compound conditioning, again a result indicating a strengthened negative hedonic reactivity compared to animals experiencing odor aversion conditioning alone. Taken together, these results indicate that taste-mediated potentiation of odor aversion conditioning impacts on the acquisition of conditioned hedonic reactions as well as consumption.

Effects of flavour variety on the intake and palatability of commercial feed in nursery pigs.

Sensory-specific satiety (SSS) could negatively affect pigs' feed intake, even when diets satisfy their nutritional requirements. We evaluated the short-term effects of SSS on feed intake and palatability. Thirty-two nursery pigs (tested in pairs) were exposed to short-term feeding trials for 6 days. In Trial 1, animals received for 90 min over three consecutive days three feeders: with different flavours (VAR); the same flavour (MON); or a mixture of the three flavours (MIX) in a 3 × 3 Latin square design. In Trial 2, with the same animals and different flavours, the three feeders were delivered successively (1 feeder every 30 min). In Trial 1, there was a day-by-diet interaction (F 4,36 = 2.98; p = 0.032), where the VAR diet was least consumed on the first day but most consumed subsequently. In Trial 2 a triple interaction between diet, day and delivery order modified pig's intake (F 12,15 = 3.33; p = 0.015), and consumption patterns (F 12,15 = 3.52; p = 0.012); where VAR diet presented the highest values in the last delivery order on the third experimental day. Flavour variety may decrease the effect of SSS, increasing feed intake and hedonic value in nursery pigs when there was a previous experience with those flavours.

A mild impairment in reversal learning in a bowl-digging substrate deterministic task but not other cognitive tests in the Dlg2+/- rat model of genetic risk for psychiatric disorder.

Variations in the Dlg2 gene have been linked to increased risk for psychiatric disorders, including schizophrenia, autism spectrum disorders, intellectual disability, bipolar disorder, attention deficit hyperactivity disorder, and pubertal disorders. Recent studies have reported disrupted brain circuit function and behaviour in models of Dlg2 knockout and haploinsufficiency. Specifically, deficits in hippocampal synaptic plasticity were found in heterozygous Dlg2+/- rats suggesting impacts on hippocampal dependent learning and cognitive flexibility. Here, we tested these predicted effects with a behavioural characterisation of the heterozygous Dlg2+/- rat model. Dlg2+/- rats exhibited a specific, mild impairment in reversal learning in a substrate deterministic bowl-digging reversal learning task. The performance of Dlg2+/- rats in other bowl digging task, visual discrimination and reversal, novel object preference, novel location preference, spontaneous alternation, modified progressive ratio, and novelty-suppressed feeding test were not impaired. These findings suggest that despite altered brain circuit function, behaviour across different domains is relatively intact in Dlg2+/- rats, with the deficits being specific to only one test of cognitive flexibility. The specific behavioural phenotype seen in this Dlg2+/- model may capture features of the clinical presentation associated with variation in the Dlg2 gene.

Face masks have emotion-dependent dissociable effects on accuracy and confidence in identifying facial expressions of emotion.

The coronavirus pandemic has resulted in increased use of face masks worldwide. Here, we examined the effect of wearing a face mask on the ability to recognise facial expressions of emotion. In a within-subjects design, 100 UK-based undergraduate students were shown facial expressions of anger, disgust, fear, happiness, sadness, and neutral expression; these were either posed with or without a face mask, or with a face mask artificially imposed onto them. Participants identified the emotion portrayed in the photographs from a fixed choice array of answers and rated their confidence in their selection. While overall accuracy was higher without than with masks, the effect varied across emotions, with a clear advantage without masks in disgust, happiness, and sadness; no effect for neutral, and lower accuracy without masks for anger and fear. In contrast, confidence was generally higher without masks, with the effect clear for all emotions other than anger. These results confirm that emotion recognition is affected by face mask wearing, but reveal that the effect depends on the emotion being displayed-with this emotion-dependence not reflected in subjects' confidence. The disparity between the effects of mask wearing on different emotions and the failure of this to be reflected in confidence ratings suggests that mask wearing not only effects emotion recognition, but may also create biases in the perception of facial expressions of emotion of which perceivers are unaware. In addition, the similarity of results between the Imposed Mask and Posed Mask conditions suggests that prior research using artificially imposed masks has not been deleteriously affected by the use of this manipulation.

Associative change in Pavlovian conditioning: A reappraisal.

Robert A. Rescorla changed how Pavlovian conditioning was studied and interpreted. His empirical contributions were fundamental and theoretically driven. One involved testing a central tenet of the model that he developed with Allan R. Wagner. The Rescorla-Wagner learning rule uses a pooled error term to determine changes in a directional association between the representations of the conditioned stimulus (CS) and unconditioned stimulus (US). This learning rule predicts that 2 equally salient CSs (A and B) will undergo equivalent associative change when they are conditioned in compound (i.e., AB→US). Rescorla's results suggested that this was not the case (e.g., Rescorla, 2000). Here, we show that these results can be reconciled with a model that uses a learning rule with a pooled error term once that rule is applied equivalently to all of the stimuli presented on a given trial, and the resulting reciprocal associations (directly and indirectly) contribute to performance. This model, called HeiDI, integrates several features of Rescorla's research and theorizing while addressing an issue that he recognized required further analysis: how learning is translated into performance. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Higher-order conditioning: A critical review and computational model.

Higher-order conditioning results from a simple training procedure: Pairing two relatively neutral conditioned stimuli, A and X, allows properties separately conditioned to X (e.g., through pairing it with an unconditioned stimulus, US) to be evident during A. The phenomenon extends the range of ways in which Pavlovian conditioned responding can be expressed and increases its translational relevance. Given this relevance and the wealth of available behavioral analysis, it is a surprisingly underdeveloped territory for formal theoretical analysis. Here, we first provide a critical review of two (informal) classes of account for higher-order conditioning that reflect either: (a) processes that are analogous to Pavlovian conditioning, but involving associatively activated representations (e.g., A→US); or (b) the formation of an associative chain (e.g., A→X, and X→US). Our review first identifies fundamental theoretical and empirical challenges to both classes of account. We then develop a new computational model of higher-order conditioning that meets the challenges identified by showing: how reciprocal associations between A, X, and the US are formed and affect performance; and how the similarity of stimuli, their traces, and associatively retrieved representations modulate this process. The model generates a wealth of novel predictions, providing a platform for further empirical and theoretical analysis. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Perceptual learning after rapidly alternating exposure to taste compounds: Assessment with different indices of generalization.

Exposure to two similar stimuli (AX and BX; e.g., two tastes) reduces the extent to which a conditioned response later established to BX generalizes to AX. This example of perceptual learning is more evident when AX and BX are exposed in an alternating manner (AX, BX, AX, BX,…) than when AX and BX occur in separate blocks (e.g., AX, AX,…BX, BX,…). We examined in male rats (N = 126) the impact of rapid alternation to AX and BX on generalization of a taste aversion from BX to AX. Experiment 1 showed that such alternating presentations (with 5-min intervals between AX and BX) reduced generalization relative to blocked exposure; but only as assessed by consumption levels and not by lick cluster size (an index of hedonic reactions). Experiment 1 also showed that the nature of exposure did not affect how A influenced performance to a novel conditioned taste, Y. Experiment 2 replicated the pattern of results involving the different influences of rapidly alternating and blocked exposure on generalization from BX to AX, and showed that this effect was only evident when rats received access to water during the 5-min intervals between AX and BX. These results reinforce parallels between perceptual learning effects in rats and humans, both at empirical and theoretical levels. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Characterizing Hedonic Responses to Flavors Paired with Internal Pain and Nausea through the Taste Reactivity Test in Rats.

Feeding behavior is a complex experience that involves not only sensory (i.e., visual, odor, taste, or texture) but also affective or emotional aspects (i.e., pleasure, palatability, or hedonic value) of foods. As such, behavioral tests that assess the hedonic impact of foods are necessary to fully understand the factors involved in ingestive behavior. In this protocol, we use the taste reactivity (TR) test to characterize the hedonic responses of rats to flavors paired with either lithium chloride-induced nausea or internal pain produced by hypertonic NaCl, two treatments that reduce voluntary consumption. This application of the TR test demonstrates how emetic and non-emetic (somatic pain in particular) treatments produce dissociable patterns of hedonic reactions to fluids: only emetic treatments result in the production of aversive orofacial responses, reflecting conditioned nausea, whereas somatic pain produces immobility, reflecting conditioned fear. Other methods, such as the microstructural analysis of licking behavior, do not reliably distinguish conditioned nausea and fear, a key advantage of the more selective TR procedure. This protocol also contains guidance for adaptation to other species and designs.