Effects of Experiencing CS-US Pairings on Instructed Fear Reversal.

Fear learning allows us to identify and anticipate aversive events and adapt our behavior accordingly. This is often thought to rely on associative learning mechanisms where an initially neutral conditioned stimulus (CS) is repeatedly paired with an aversive unconditioned stimulus (US), eventually leading to the CS also being perceived as aversive and threatening. Importantly, however, humans also show verbal fear learning. Namely, they have the ability to change their responses to stimuli rapidly through verbal instructions about CS-US pairings. Past research on the link between experience-based and verbal fear learning indicated that verbal instructions about a reversal of CS-US pairings can fully override the effects of previously experienced CS-US pairings, as measured through fear ratings, skin conductance, and fear-potentiated startle. However, it remains an open question whether such instructions can also annul learned CS representations in the brain. Here, we used a fear reversal paradigm (female and male participants) in conjunction with representational similarity analysis of fMRI data to test whether verbal instructions fully override the effects of experienced CS-US pairings in fear-related brain regions or not. Previous research suggests that only the right amygdala should show lingering representations of previously experienced threat ("pavlovian trace"). Unexpectedly, we found evidence for the residual effect of prior CS-US experience to be much more widespread than anticipated, in the amygdala but also cortical regions like the dorsal anterior cingulate or dorsolateral prefrontal cortex. This finding shines a new light on the interaction of different fear learning mechanisms, at times with unexpected consequences.SIGNIFICANCE STATEMENT Humans are able to learn about aversive stimuli both from experience (i.e., repeated pairings of conditioned stimulus (CS) and unconditioned stimulus (US; pavlovian conditioning), and from verbal instructions about stimulus pairings. Understanding how experience-based and verbal learning processes interact is key for understanding the cognitive and neural underpinnings of fear learning. We tested whether prior aversive experiences (CS-US pairings) affected subsequent verbal learning, searching for lingering threat signals after verbal instructions reversed a CS from being threatening to being safe. While past research suggested such threat signals can only be found in the amygdala, we found evidence to be much more widespread, including the medial and lateral PFC. This highlights how experience-based and verbal learning processes interact to support adaptive behavior.

Regulation of the Ca2+ Channel CaV1.2 Supports Spatial Memory and Its Flexibility and LTD.

Widespread release of norepinephrine (NE) throughout the forebrain fosters learning and memory via adrenergic receptor (AR) signaling, but the molecular mechanisms are largely unknown. The ß2 AR and its downstream effectors, the trimeric stimulatory Gs-protein, adenylyl cyclase (AC), and the cAMP-dependent protein kinase A (PKA), form a unique signaling complex with the L-type Ca2+ channel (LTCC) CaV1.2. Phosphorylation of CaV1.2 by PKA on Ser1928 is required for the upregulation of Ca2+ influx on ß2 AR stimulation and long-term potentiation induced by prolonged theta-tetanus (PTT-LTP) but not LTP induced by two 1-s-long 100-Hz tetani. However, the function of Ser1928 phosphorylation in vivo is unknown. Here, we show that S1928A knock-in (KI) mice of both sexes, which lack PTT-LTP, express deficiencies during initial consolidation of spatial memory. Especially striking is the effect of this mutation on cognitive flexibility as tested by reversal learning. Mechanistically, long-term depression (LTD) has been implicated in reversal learning. It is abrogated in male and female S1928A knock-in mice and by ß2 AR antagonists and peptides that displace ß2 AR from CaV1.2. This work identifies CaV1.2 as a critical molecular locus that regulates synaptic plasticity, spatial memory and its reversal, and LTD.SIGNIFICANCE STATEMENT We show that phosphorylation of the Ca2+ channel CaV1.2 on Ser1928 is important for consolidation of spatial memory and especially its reversal, and long-term depression (LTD). Identification of Ser1928 as critical for LTD and reversal learning supports the model that LTD underlies flexibility of reference memory.

Poly (I:C)-induced maternal immune activation generates impairment of reversal learning performance in offspring.

Maternal immune activation (MIA) induces a variety of behavioral and brain abnormalities in offspring of rodent models, compatible with neurodevelopmental disorders, such as schizophrenia or autism. However, it remains controversial whether MIA impairs reversal learning, a basic expression of cognitive flexibility that seems to be altered in schizophrenia. In the present study, MIA was induced by administration of a single dose of polyriboinosinic-polyribocytidylic acid (Poly (I:C) (5 mg/kg i.p.)) or saline to mouse pregnant dams in gestational day (GD) 9.5. Immune activation was monitored through changes in weight and temperature. The offspring were evaluated when they reached adulthood (8 weeks) using a touchscreen-based system to investigate the effects of Poly (I:C) on discrimination and reversal learning performance. After an initial pre-training, mice were trained to discriminate between two different stimuli, of which only one was rewarded (acquisition phase). When the correct response reached above 80% values for two consecutive days, the images were reversed (reversal phase) to assess the adaptation capacity to a changing environment. Maternal Poly (I:C) treatment did not interfere with the learning process but induced deficits in reversal learning compared to control saline animals. Thus, the accuracy in the reversal phase was lower, and Poly (I:C) animals required more sessions to complete it, suggesting impairments in cognitive flexibility. This study advances the knowledge of how MIA affects behavior, especially cognitive domains that are impaired in schizophrenia. The findings support the validity of the Poly (I:C)-based MIA model as a tool to develop pharmacological treatments targeting cognitive deficits associated with neurodevelopmental disorders.

Sex-dependent differences in the ability of nicotine to modulate discrimination learning and cognitive flexibility in mice.

Nicotine, an addictive compound found in tobacco, functions as an agonist of nicotinic acetylcholine receptors (nAChRs) in the brain. Interestingly, nicotine has been reported to act as a cognitive enhancer in both human subjects and experimental animals. However, its effects in animal studies have not always been consistent, and sex differences have been identified in the effects of nicotine on several behaviors. Specifically, the role that sex plays in modulating the effects of nicotine on discrimination learning and cognitive flexibility in rodents is still unclear. Here, we evaluated sex-dependent differences in the effect of daily nicotine intraperitoneal (i.p.) administration at various doses (0.125, 0.25, and 0.5 mg/kg) on visual discrimination (VD) learning and reversal (VDR) learning in mice. In male mice, 0.5 mg/kg nicotine significantly improved performance in the VDR, but not the VD, task, while 0.5 mg/kg nicotine significantly worsened performance in the VD, but not VDR task in female mice. Furthermore, 0.25 mg/kg nicotine significantly worsened performance in the VD and VDR task only in female mice. Next, to investigate the cellular mechanisms that underlie the sex difference in the effects of nicotine on cognition, transcriptomic analyses were performed focusing on the medial prefrontal cortex tissue samples from male and female mice that had received continuous administration of nicotine for 3 or 18 days. As a result of pathway enrichment analysis and protein-protein interaction analysis using gene sets of differentially expressed genes, decreased expression of postsynaptic-related genes in males and increased expression of innate immunity-related genes in females were identified as possible molecular mechanisms related to sex differences in the effects of nicotine on cognition in discrimination learning and cognitive flexibility. Our result suggests that nicotine modulates cognitive function in a sex-dependent manner by alternating the expression of specific gene sets in the medial prefrontal cortex.

The medial prefrontal cortex during flexible decisions: Evidence for its role in distinct working memory processes.

During decisions that involve working memory, task-related information must be encoded, maintained across delays, and retrieved. Few studies have attempted to causally disambiguate how different brain structures contribute to each of these components of working memory. In the present study, we used transient optogenetic disruptions of rat medial prefrontal cortex (mPFC) during a serial spatial reversal learning (SSRL) task to test its role in these specific working memory processes. By analyzing numerous performance metrics, we found: (1) mPFC disruption impaired performance during only the choice epoch of initial discrimination learning of the SSRL task; (2) mPFC disruption impaired performance in dissociable ways across all task epochs (delay, choice, return) during flexible decision-making; (3) mPFC disruption resulted in a reduction of the typical vicarious-trial-and-error rate modulation that was related to changes in task demands. Taken together, these findings suggest that the mPFC plays an outsized role in working memory retrieval, becomes involved in encoding and maintenance when recent memories conflict with task demands, and enables animals to flexibly utilize working memory to update behavior as environments change.

Cognitive flexibility in urban yellow mongooses, Cynictis penicillata.

Cognitive flexibility enables animals to alter their behaviour and respond appropriately to environmental changes. Such flexibility is important in urban settings where environmental changes occur rapidly and continually. We studied whether free-living, urban-dwelling yellow mongooses, Cynictis penicillata, in South Africa, are cognitively flexible in reversal learning and attention task experiments (n = 10). Reversal learning was conducted using two puzzle boxes that were distinct visually and spatially, each containing a preferred or non-preferred food type. Once mongooses learned which box contained the preferred food type, the food types were reversed. The mongooses successfully unlearned their previously learned response in favour of learning a new response, possibly through a win-stay, lose-shift strategy. Attention task experiments were conducted using one puzzle box surrounded by zero, one, two or three objects, introducing various levels of distraction while solving the task. The mongooses were distracted by two and three distractions but were able to solve the task despite the distractions by splitting their attention between the puzzle box task and remaining vigilant. However, those exposed to human residents more often were more vigilant. We provide the first evidence of cognitive flexibility in urban yellow mongooses, which enables them to modify their behaviour to urban environments.

Serial visual reversal learning in captive black-handed spider monkeys, Ateles geoffroyi.

Recent research suggests that socio-ecological factors such as dietary specialization and social complexity may be drivers of advanced cognitive skills among primates. Therefore, we assessed the ability of 12 black-handed spider monkeys (Ateles geoffroyi), a highly frugivorous platyrrhine primate with strong fission-fusion dynamics, to succeed in a serial visual reversal learning task. Using a two-alternative choice paradigm we first trained the animals to reliably choose a rewarded visual stimulus over a non-rewarded one. Upon reaching a pre-set learning criterion we then switched the reward values of the two stimuli and assessed if and how quickly the animals learned to reverse their choices, again to a pre-set learning criterion. This stimulus reversal procedure was then continued for a total of 80 sessions of 10 trials each. We found that the spider monkeys quickly learned to reliably discriminate between two simultaneously presented visual stimuli, that they succeeded in a visual reversal learning task, and that they displayed an increase in learning speed across consecutive reversals, suggesting that they are capable of serial reversal learning-set formation with visual cues. The fastest-learning individual completed five reversals within the 80 sessions. The spider monkeys outperformed most other primate and nonprimate mammal species tested so far on this type of cognitive task, including chimpanzees, with regard to their learning speed in both the initial learning task and in the first reversal task, suggesting a high degree of behavioral flexibility and inhibitory control. Our findings support the notion that socio-ecological factors such as dietary specialization and social complexity foster advanced cognitive skills in primates.

Serial reversal learning in nectar-feeding bats.

We explored the behavioral flexibility of Commissaris's long-tongued bats through a spatial serial reversal foraging task. Bats kept in captivity for short periods were trained to obtain nectar rewards from two artificial flowers. At any given time, only one of the flowers provided rewards and these reward contingencies reversed in successive blocks of 50 flower visits. All bats detected and responded to reversals by making most of their visits to the currently active flower. As the bats experienced repeated reversals, their preference re-adjusted faster. Although the flower state reversals were theoretically predictable, we did not detect anticipatory behavior, that is, frequency of visits to the alternative flower did not increase within each block as the programmed reversal approached. The net balance of these changes was a progressive improvement in performance in terms of the total proportion of visits allocated to the active flower. The results are compatible with, but do not depend on, the bats displaying an ability to 'learn to learn' and show that the dynamics of allocation of effort between food sources can change flexibly according to circumstances.

Dorsal posterior cingulate cortex responds to negative feedback information supporting learning and relearning of response policies.

Many challenges in life come without explicit instructions. Instead, humans need to test, select, and adapt their behavioral responses based on feedback from the environment. While reward-centric accounts of feedback processing primarily stress the reinforcing aspect of positive feedback, feedback's central function from an information-processing perspective is to offer an opportunity to correct errors, thus putting a greater emphasis on the informational content of negative feedback. Independent of its potential rewarding value, the informational value of performance feedback has recently been suggested to be neurophysiologically encoded in the dorsal portion of the posterior cingulate cortex (dPCC). To further test this association, we investigated multidimensional categorization and reversal learning by comparing negative and positive feedback in an event-related functional magnetic resonance imaging experiment. Negative feedback, compared with positive feedback, increased activation in the dPCC as well as in brain regions typically involved in error processing. Only in the dPCC, subarea d23, this effect was significantly enhanced in relearning, where negative feedback signaled the need to shift away from a previously established response policy. Together with previous findings, this result contributes to a more fine-grained functional parcellation of PCC subregions and supports the dPCC's involvement in the adaptation to behaviorally relevant information from the environment.

Fecal microbiota transplantation of patients with anorexia nervosa did not alter flexible behavior in rats.

OBJECTIVE: Patients with anorexia nervosa (AN) are often anxious, display inflexible behavior and disrupted reward processing. Emerging evidence suggests that gut dysbiosis in patients contributes to the disease phenotype and progression. METHODS: In a preclinical study, we explored whether AN-derived microbiota impacts cognitive flexibility, anxiety, and dopamine signaling using fecal microbiota transplantation (FMT) in tyrosine hydroxylase-cre rats. We performed probabilistic reversal learning task (PRLT) at the baseline, after antibiotic treatment, and following FMT from patients with AN and controls. We assessed flexible behavior, task engagement, and ventral tegmental area (VTA) dopamine signaling during and in the absence of reward. Furthermore, anxiety-like behavior was evaluated with open field (OF) and elevated plus maze (EPM) tests. RESULTS: Neither antibiotic-induced dysbiosis nor AN FMT led to significant alterations in the number of reversals or lever press strategies after reinforced or nonreinforced lever presses (win and lose-stay) in the PRLT. However, the number of initiated trials decreased after antibiotic treatment while remaining unchanged after FMT. No significant differences were observed in VTA dopamine activity, anxiety measures in the OF and EPM tests. Microbiome analysis revealed limited overlap between the microbiota of the donors and recipients. DISCUSSION: No evidence was found that the microbiota of patients compared to controls, nor a depleted microbiome impacts cognitive flexibility. Nonetheless, antibiotic-induced dysbiosis resulted in reduced task engagement during the PRLT. The relatively low efficiency of the FMT is a limitation of our study and highlights the need for improved protocols to draw robust conclusions in future studies. PUBLIC SIGNIFICANCE: While our study did not reveal direct impacts of AN-associated gut microbiota on cognitive flexibility or anxiety behaviors in our preclinical model, we observed a decrease in task engagement after antibiotic-induced dysbiosis, underscoring that the presence of a gut microbiome matters. Our findings underscore the need for further refinement in FMT protocols to better elucidate the complex interplay between gut microbiota and behaviors characteristic of anorexia nervosa.

Going back to "basics": Harlow's learning set task with wolves and dogs.

To survive and reproduce, animals need to behave adaptively by adjusting their behavior to their environment, with learning facilitating some of these processes. Dogs have become a go-to model species in comparative cognition studies, making our understanding of their learning skills paramount at multiple levels, not only with regards to basic research on their cognitive skills and the effects of domestication, but also with applied purposes such as training. In order to tackle these issues, we tested similarly raised wolves and dogs in a serial learning task inspired by Harlow's "learning set." In Phase 1, different pairs of objects were presented to the animals, one of which was baited while the other was not. Both species' performance gradually improved with each new set of objects, showing that they "learnt to learn," but no differences were found between the species in their learning speed. In Phase 2, once subjects had learned the association between one of the objects and the food reward, the contingencies were reversed and the previously unrewarded object of the same pair was now rewarded. Dogs' performance in this task seemed to be better than wolves', albeit only when considering just the first session of each reversal, suggesting that the dogs might be more flexible than wolves. Further research (possibly with the aid of refined methods such as computer-based tasks) would help ascertain whether these differences between wolves and dogs are persistent across different learning tasks.

Coercive mating has no impact on spatial learning, cognitive flexibility, and fecundity in female porthole livebearers (Poeciliopsis gracilis).

Coercive mating is a sexual selection strategy that is likely to influence female cognition. Female harassment levels have been linked to altered brain gene expression patterns and brain size evolution, suggesting females may respond to coercive mating by investing energy into "outsmarting" males. However, females exposed to coercive males have decreased foraging efficiency and likely increased stress levels, suggesting their brain function might instead be impaired. While it is therefore likely that coercive mating impacts female cognitive abilities, a direct test of this idea is currently lacking. In this study, we investigate the impact of coercive mating on female spatial memory and cognitive flexibility in a species with prevalent coercive mating. We compared the performance of female porthole livebearers (Poeciliopsis gracilis), which had been previously housed alone or with a coercive male, in both a spatial food localization task and a reversal learning task. While we found that both single and paired fish exhibited high proficiency in learning both tasks, we found no differences in learning ability between females that had or had not experienced coercive mating. In addition, our study found that the presence of a coercive male had no impact on female fecundity, but did influence female mass and standard length. Several studies have assumed that the presence of males, particularly coercive males, may affect the cognitive performance of female fish. However, our study shows that for some species females adapted to coercive mating regimes may be unaffected by male presence with regards to some cognitive tasks.

Neuropharmacological Evidence Implicating Drug-Induced Glutamate Receptor Dysfunction in Affective and Cognitive Sequelae of Subchronic Methamphetamine Self-Administration in Mice.

Methamphetamine (MA) is a highly addictive drug, and MA use disorder is often comorbid with anxiety and cognitive impairment. These comorbid conditions are theorized to reflect glutamate-related neurotoxicity within the frontal cortical regions. However, our prior studies of MA-sensitized mice indicate that subchronic, behaviorally non-contingent MA treatment is sufficient to dysregulate glutamate transmission in mouse brain. Here, we extend this prior work to a mouse model of high-dose oral MA self-administration (0.8, 1.6, or 3.2 g/L; 1 h sessions × 7 days) and show that while female C57BL/6J mice consumed more MA than males, MA-experienced mice of both sexes exhibited some signs of anxiety-like behavior in a behavioral test battery, although not all effects were concentration-dependent. No MA effects were detected for our measures of visually cued spatial navigation, spatial learning, or memory in the Morris water maze; however, females with a history of 3.2 g/L MA exhibited reversal-learning deficits in this task, and mice with a history of 1.6 g/L MA committed more working-memory incorrect errors and relied upon a non-spatial navigation strategy during the radial-arm maze testing. Relative to naïve controls, MA-experienced mice exhibited several changes in the expression of certain glutamate receptor-related proteins and their downstream effectors within the ventral and dorsal areas of the prefrontal cortex, the hippocampus, and the amygdala, many of which were sex-selective. Systemic pretreatment with the mGlu1-negative allosteric modulator JNJ 162596858 reversed the anxiety-like behavior expressed by MA-experienced mice in the marble-burying test, while systemic pretreatment with NMDA or the NMDA antagonist MK-801 bi-directionally affected the MA-induced reversal-learning deficit. Taken together, these data indicate that a relatively brief history of oral MA is sufficient to induce some signs of anxiety-like behavior and cognitive dysfunction during early withdrawal that reflect, at least in part, MA-induced changes in the corticolimbic expression of certain glutamate receptor subtypes of potential relevance to treating symptoms of MA use disorder.

GoFish: A low-cost, open-source platform for closed-loop behavioural experiments on fish.

Fish are the most species-rich vertebrate group, displaying vast ecological, anatomical and behavioural diversity, and therefore are of major interest for the study of behaviour and its evolution. However, with respect to other vertebrates, fish are relatively underrepresented in psychological and cognitive research. A greater availability of easily accessible, flexible, open-source experimental platforms that facilitate the automation of task control and data acquisition may help to reduce this bias and improve the scalability and refinement of behavioural experiments in a range of different fish species. Here we present GoFish, a fully automated platform for behavioural experiments in aquatic species. GoFish includes real-time video tracking of subjects, presentation of stimuli in a computer screen, an automatic feeder device, and closed-loop control of task contingencies and data acquisition. The design and software components of the platform are freely available, while the hardware is open-source and relatively inexpensive. The control software, Bonsai, is designed to facilitate rapid development of task workflows and is supported by a growing community of users. As an illustration and test of its use, we present the results of two experiments on discrimination learning, reversal, and choice in goldfish (Carassius auratus). GoFish facilitates the automation of high-throughput protocols and the acquisition of rich behavioural data. Our platform has the potential to become a widely used tool that facilitates complex behavioural experiments in aquatic species.

Silencing hippocampal CA2 reduces behavioral flexibility in spatial learning.

The hippocampus is a key structure involved in learning and remembering spatial information. However, the extent to which hippocampal region CA2 is involved in these processes remains unclear. Here, we show that chronically silencing dorsal CA2 impairs reversal learning in the Morris water maze. After platform relocation, CA2-silenced mice spent more time in the vicinity of the old platform location and less time in the new target quadrant. Accordingly, behavioral strategy analysis revealed increased perseverance in navigating to the old location during the first day and an increased use of non-spatial strategies during the second day of reversal learning. Confirming previous indirect indications, these results demonstrate that CA2 is recruited when mice must flexibly adapt their behavior as task contingencies change. We discuss how these findings can be explained by recent theories of CA2 function and outline testable predictions to understand the underlying neural mechanisms. Demonstrating a direct involvement of CA2 in spatial learning, this work lends further support to the notion that CA2 plays a fundamental role in hippocampal information processing.

Characterization of striatal dopamine projections across striatal subregions in behavioral flexibility.

Behavioural flexibility is key to survival in a dynamic environmentWhile flexible, goal-directed behaviours are initially dependent on dorsomedial striatum, they become dependent on lateral striatum as behaviours become inflexible. Similarly, lesions of dopamine terminals in lateral striatum disrupt the development of inflexible habits. This work suggests that dopamine release in lateral striatum may drive inflexible behaviours, though few studies have investigated a causative role of subpopulations of striatal dopamine terminals in reversal learning, a measure of flexibility. Here, we performed two optogenetic experiments to activate dopamine terminals in dorsomedial (DMS), dorsolateral (DLS) or ventral (nucleus accumbens [NAc]) striatum in DAT-Cre mice that expressed channelrhodopsin-2 via viral injection (Experiment I) or through transgenic breeding with an Ai32 reporter line (Experiment II) to determine how specific dopamine subpopulations impact reversal learning. Mice performed a reversal task in which they self-stimulated DMS, DLS, or NAc dopamine terminals by pressing one of two levers before action-outcome lever contingencies were reversed. Largely consistent with presumed ventromedial/lateral striatal function, we found that mice self-stimulating medial dopamine terminals reversed lever preference following contingency reversal, while mice self-stimulating NAc showed parial flexibility, and DLS self-stimulation resulted in impaired reversal. Impairments in DLS mice were characterized by more regressive errors and reliance on lose-stay strategies following reversal, as well as reduced within-session learning, suggesting reward insensitivity and overreliance on previously learned actions. This study supports a model of striatal function in which DMS and ventral dopamine facilitate goal-directed responding, and DLS dopamine supports more inflexible responding.

How uncertain are you? Disentangling expected and unexpected uncertainty in pupil-linked brain arousal during reversal learning.

During decision making, we are continuously faced with two sources of uncertainty regarding the links between stimuli, our actions, and outcomes. On the one hand, our expectations are often probabilistic, that is, stimuli or actions yield the expected outcome only with a certain probability (expected uncertainty). On the other hand, expectations might become invalid due to sudden, unexpected changes in the environment (unexpected uncertainty). Several lines of research show that pupil-linked brain arousal is a sensitive indirect measure of brain mechanisms underlying uncertainty computations. Thus, we investigated whether it is involved in disentangling these two forms of uncertainty. To this aim, we measured pupil size during a probabilistic reversal learning task. In this task, participants had to figure out which of two response options led to reward with higher probability, whereby sometimes the identity of the more advantageous response option was switched. Expected uncertainty was manipulated by varying the reward probability of the advantageous choice option, whereas the level of unexpected uncertainty was assessed by using a Bayesian computational model estimating change probability and resulting uncertainty. We found that both aspects of unexpected uncertainty influenced pupil responses, confirming that pupil-linked brain arousal is involved in model updating after unexpected changes in the environment. Furthermore, high level of expected uncertainty impeded the detection of sudden changes in the environment, both on physiological and behavioral level. These results emphasize the role of pupil-linked brain arousal and underlying neural structures in handling situations in which the previously established contingencies are no longer valid.

Artificial selection for reversal learning reveals limited repeatability and no heritability of cognitive flexibility in great tits (Parus major).

Cognitive flexibility controls how animals respond to changing environmental conditions. Individuals within species vary considerably in cognitive flexibility but the micro-evolutionary potential in animal populations remains enigmatic. One prerequisite for cognitive flexibility to be able to evolve is consistent and heritable among-individual variation. Here we determine the repeatability and heritability of cognitive flexibility among great tits (Parus major) by performing an artificial selection experiment on reversal learning performance using a spatial learning paradigm over three generations. We found low, yet significant, repeatability (R = 0.15) of reversal learning performance. Our artificial selection experiment showed no evidence for narrow-sense heritability of associative or reversal learning, while we confirmed the heritability of exploratory behaviour. We observed a phenotypic, but no genetic, correlation between associative and reversal learning, showing the importance of prior information on reversal learning. We found no correlation between cognitive and personality traits. Our findings emphasize that cognitive flexibility is a multi-faceted trait that is affected by memory and prior experience, making it challenging to retrieve reliable values of temporal consistency and assess the contribution of additive genetic variation. Future studies need to identify what cognitive components underlie variation in reversal learning and study their between-individual and additive genetic components.

Effects of early-life stress on probabilistic reversal learning and response perseverance in young adults.

Early life stress (ELS), including experiences with abuse and neglect, are related to several negative health outcomes in adulthood. One area that has received attention is the increased rate of substance abuse disorder in individuals who had experienced ELS. Given the critical role habitual behavior in the development of substance abuse, ELS may affect the trajectory of neural development such that habitual responding is more dominant than in individuals who did not experience ELS. Here, we examine learning of a probabilistic classification task (the Weather Prediction Task) in healthy young adults who reported significant ELS and those that did not. This task can be learned in a declarative, model-based manner, or in a more habitual, stimulus-response manner. Participants learned to choose the outcome (sun or rain) that was probabilistically associated with each cue combination through reinforcement on each trial. After 100 trials, the probabilities were reversed, and we conceptualized habitual behavior as perseverating responses based on the old probabilities. We also collected information about subjective socio-economic status (sSES), anxiety, depression, and substance use from participants. Using multiple regression, we found that our measure of habitual responding was correlated with reported alcohol use, suggesting that our measure of habit has validity for health behaviors. Furthermore, we found that some forms of early life stress led to greater response perseverance after contingencies were reversed. Overall, the results suggest that childhood adversity may contribute to the development of habit.

Assessing sex differences in behavioural flexibility in an endangered bird species: the Southern ground-hornbill (Bucorvus leadbeateri).

Since ecology influences the expression of cognitive traits, intra-specific variation in ecological demands can drive differences in cognition. This is often the case, for instance, when sexes face different ecological challenges. However, so far, most studies have focused on few cognitive domains (i.e., spatial cognition), which limits our understanding of the evolution of sexually dimorphic cognition in animals. Endangered Southern ground-hornbills (Bucorvus leadbeateri), for example, show sex-specific ecological differences in age at dispersal, where females disperse from their natal group earlier than males. Based on this potential sex-specific source of selection, females and males may differ in their capacity to behave flexibly. Here, we used the reversal-learning paradigm in ten Southern ground-hornbills in two conditions: spatial and colour. During the pre-test (learning phase), regardless the sex, all subjects were faster at associating the food reward with spatial rather than with colour cues. Similarly, during the test (reversal-learning phase), both sexes learned the new association quicker with spatial cues. There were no sex differences in learning or reversal learning during both experimental phases. This possibility, however, requires further observation and experimentation. We hope our study will provide the impetus to assess further the cognitive capacities of this still overlooked species.