Discrimination reversal learning reveals greater female behavioural flexibility in guppies
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ABSTRACT:
SUBMITTER: Lucon-Xiccato T
PROVIDER: S-EPMC4090544 | biostudies-literature | 2014 Jun
REPOSITORIES: biostudies-literature
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Project description:Cognitive flexibility describes the ability of animals to alter cognitively mediated behaviour in response to changing situational demands, and can vary according to prevailing environemental conditions and individual caracteristics. In the present study, we investigated (1) how learning and reversal learning performance changes between seasons, and (2) how cognitive flexibility is related to sex in a free-living small mammal. We studied 107 African striped mice, Rhabdomys pumilio, in an arid semi-desert, 58 during the hot dry summer with low food availability, and 49 during the cold wet winter with higher food availability. We used an escape box task to test for learning and reversal learning performance. We found that learning and reversal learning efficiency varied seasonally by sex: females tested in summer were faster at solving both learning and reversal tasks than males tested in winter. Performance varied within sex: males tested in winter showed faster learning compared to males tested in summer. During reversal learning, females tested in summer were more efficient and solve the task faster compared to females tested in winter. We suggest that seasonal cognitive performance could be related to sex-specific behavioural characteristics of the species, resulting in adaptation for living in harsh environmental conditions.
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Project description:Behavioral inflexibility is a feature of schizophrenia, attention-deficit/hyperactivity disorder, and behavior addictions that likely results from heritable deficits in the inhibitory control over behavior. Here, we investigate the genetic basis of individual differences in flexibility, measured using an operant reversal learning task.We quantified discrimination acquisition and subsequent reversal learning in a cohort of 51 BXD strains of mice (2-5 mice/strain, n = 176) for which we have matched data on sequence, gene expression in key central nervous system regions, and neuroreceptor levels.Strain variation in trials to criterion on acquisition and reversal was high, with moderate heritability (?.3). Acquisition and reversal learning phenotypes did not covary at the strain level, suggesting that these traits are effectively under independent genetic control. Reversal performance did covary with dopamine D2 receptor levels in the ventral midbrain, consistent with a similar observed relationship between impulsivity and D2 receptors in humans. Reversal, but not acquisition, is linked to a locus on mouse chromosome 10 with a peak likelihood ratio statistic at 86.2 megabase (p < .05 genome-wide). Variance in messenger RNA levels of select transcripts expressed in neocortex, hippocampus, and striatum correlated with the reversal learning phenotype, including Syn3, Nt5dc3, and Hcfc2.This work demonstrates the clear trait independence between, and genetic control of, discrimination acquisition and reversal and illustrates how globally coherent data sets for a single panel of highly related strains can be interrogated and integrated to uncover genetic sources and molecular and neuropharmacological candidates of complex behavioral traits relevant to human psychopathology.
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Project description:The ability to flexibly respond to changes in the environment is critical for adaptive behavior. Reversal learning (RL) procedures test adaptive response updating when contingencies are altered. We used functional magnetic resonance imaging to examine brain areas that support specific RL components. We compared neural responses to RL and initial learning (acquisition) to isolate reversal-related brain activation independent of cognitive control processes invoked during initial feedback-based learning. Lateral orbitofrontal cortex (OFC) was more activated during reversal than acquisition, suggesting its relevance for reformation of established stimulus-response associations. In addition, the dorsal anterior cingulate (dACC) and right inferior frontal gyrus (rIFG) correlated with change in postreversal accuracy. Because optimal RL likely requires suppression of a prior learned response, we hypothesized that similar regions serve both response inhibition (RI) and inhibition of learned associations during reversal. However, reversal-specific responding and stopping (requiring RI and assessed via the stop-signal task) revealed distinct frontal regions. Although RI-related regions do not appear to support inhibition of prepotent learned associations, a subset of these regions, dACC and rIFG, guide actions consistent with current reward contingencies. These regions and lateral OFC represent distinct neural components that support behavioral flexibility important for adaptive learning.
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Project description:Background: Loss of FMR1 is associated with Fragile X syndrome, amongst the most prevalent inherited intellectual disability. Despite extensive research in this area, previous studies have failed to detect consistent evidence of cognitive impairments in the Morris water maze (MWM) task in the Fmr1 knockout (KO) mouse. However, few studies have examined cognitive flexibility in a reversal form of the MWM task, which may illuminate subtle learning deficits. Methods: Adult male Fmr1 wildtype (WT) and KO mice were bred and tested in the MWM reversal paradigm. The testing paradigm consisted of two blocks per day, with 4 trials per block to locate a hidden platform. After the last trials on the fourth day of testing, the animals were given a probe trial with the platform removed. The following week, the location of the platform was switched to the opposite quadrant and the animals received 2 more days of testing, with 4 blocks in total. Results: As expected, Fmr1 KO mice did not display a learning deficit during the acquisition phase, F genotype (1, 24) = 0.034, p = 0.854, and performed similarly on the probe trial, F genotype (1, 23) = 0.024, p = 0.877. However, during the reversal phase of learning, Fmr1 KO mice showed deficits in their ability to learn the new location of the platform, F genotype (1, 23) = 3.93, p = 0.059. Further independent samples t-testing revealed that KO animals displayed significantly higher latency to reach the hidden platform during the third trial, t(23) = -2.96, p < 0.01. Conclusions: While previous studies have not demonstrated deficits in spatial memory in the Fmr1 KO model, it is possible that the acquisition phase of the task is less sensitive to deficits in learning. Future studies using this model to evaluate therapeutic interventions should consider utilizing the MWM reversal paradigm.
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Project description:Laterality, the division of brain functions into separate hemispheres, is widespread across animal taxa. Lateralized individuals exhibit cognitive advantages yet substantial variation in laterality exists, particularly between the sexes. Why variation is maintained is unknown as few studies consider differences in lateralized behaviours between the sexes, and their underlying selection pressures, across different contexts. We investigated if Poecilia reticulata exhibited sex differences in the direction, strength and consistency of lateralization. We assessed the turning preferences of individuals detouring around a barrier to view visual stimuli representative of different behavioural contexts: an artificial object of familiar colour, an opposite sex conspecific and a no stimulus control. While no sex differences were evident in the direction or strength of laterality, consistency in the strength of laterality varied between the sexes. Individuals of both sexes consistently detoured in one direction, but the strength of laterality exhibited by males was more predictable than females across contexts. This suggests that predictability of lateralization across ecologically relevant scenarios represents a key, but previously unexplored, source of variation between the sexes.
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Project description:The corticostriatothalamic circuit regulates learning behaviors via dopamine neurotransmission. D2 long (D2L) receptors are an isoform of dopamine D2 receptors (D2Rs) and may act mainly at postsynaptic sites. It is well known that D2Rs influence high brain functions, but the roles of individual D2R isoforms are still unclear. To assess the influence of D2L receptors in visual discrimination learning, we performed visual discrimination and reversal tasks with D2L knockout mice using a touchscreen operant system. There were no significant differences in an operant conditioning task between genotypes. However, D2L knockout mice were impaired in both visual discrimination and reversal learning tasks. D2L knockout mice were also significantly slower than wild-type mice in collecting the reward in the visual discrimination task. These results indicate that D2L receptors play an important role in visual discrimination and reversal learning.
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Project description:Several studies on age-related cognitive decline in dogs involve laboratory dogs and prolonged training. We developed two spatial tasks that required a single 1-h session. We tested 107 medium-large sized dogs: "young" (N=41, aged 2.5-6.5 years) and "old" (N=66, aged 8-14.5 years). Our results indicated that, in a discrimination learning task and in a reversal learning task, young dogs learned significantly faster than the old dogs, indicating that these two tasks could successfully be used to investigate differences in spatial learning between young and old dogs. We also provide two novel findings. First, in the reversal learning, the dogs trained based on the location of stimuli learned faster than the dogs trained based on stimulus characteristics. Most old dogs did not learn the task within our cut-off of 50 trials. Training based on an object's location is therefore more appropriate for reversal learning tasks. Second, the contrast between the response to the positive and negative stimuli was narrower in old dogs, compared to young dogs, during the reversal learning task, as well as the cognitive bias test. This measure favors comparability between tasks and between studies. Following the cognitive bias test, we could not find any indication of differences in the positive and negative expectations between young and old dogs. Taken together, these findings do not support the hypothesis that old dogs have more negative expectations than young dogs and the use of the cognitive bias test in older dogs requires further investigation.
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Project description:The midsession reversal paradigm confronts an animal with a two-choice discrimination task where the reward contingencies are reversed at the midpoint of the session. Species react to the reversal with either win-stay/lose-shift, using local information of reinforcement, or reversal estimation, using global information, e.g. time, to estimate the point of reversal. Besides pigeons, only mammalian species were tested in this paradigm so far and analyses were conducted on pooled data, not considering possible individually different responses. We tested twelve kea parrots with a 40-trial midsession reversal test and additional shifted reversal tests with a variable point of reversal. Birds were tested in two groups on a touchscreen, with the discrimination task having either only visual or additional spatial information. We used Generalized Linear Mixed Models to control for individual differences when analysing the data. Our results demonstrate that kea can use win-stay/lose-shift independently of local information. The predictors group, session, and trial number as well as their interactions had a significant influence on the response. Furthermore, we discovered notable individual differences not only between birds but also between sessions of individual birds, including the ability to quite accurately estimate the reversal position in alternation to win-stay/lose-shift. Our findings of the kea's quick and flexible responses contribute to the knowledge of diversity in avian cognitive abilities and emphasize the need to consider individuality as well as the limitation of pooling the data when analysing midsession reversal data.
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Project description:Rodent behavioral tasks are crucial to understanding the nature and underlying biology of cognition and cognitive deficits observed in psychiatric and neurological pathologies. Olfaction, as the primary sensory modality in rodents, is widely used to investigate cognition in rodents. In recent years, automation of olfactory tasks has made it possible to conduct olfactory experiments in a time- and labor-efficient manner while also minimizing experimenter-induced variability. In this study, we bring automation to the next level in two ways: First, by incorporating a radio frequency identification-based sorter that automatically isolates individuals for the experimental session. Thus, we can not only test animals during defined experimental sessions throughout the day but also prevent cagemate interference during task performance. Second, by implementing software that advances individuals to the next test stage as soon as performance criteria are reached. Thus, we can prevent overtraining, a known confounder especially in cognitive flexibility tasks. With this system in hand, we trained mice on a series of four odor pair discrimination tasks as well as their respective reversals. Due to performance-based advancement, mice normally advanced to the next stage in less than a day. Over the series of subsequent odor pair discriminations, the number of errors to criterion decreased significantly, thus indicating the formation of a learning set. As expected, errors to criterion were higher during reversals. Our results confirm that the system allows investigating higher-order cognitive functions such as learning set formation (which is understudied in mice) and reversal learning (which is a measure of cognitive flexibility and impaired in many clinical populations). Therefore, our system will facilitate investigations into the nature of cognition and cognitive deficits in pathological conditions by providing a high-throughput and labor-efficient experimental approach without the risks of overtraining or cagemate interference.
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Project description:We suggest that variation in mammalian behavioural flexibility not accounted for by current socioecological models may be explained in part by developmental constraints. From our own work, we provide examples of constraints affecting variation in behavioural flexibility, not only among individuals, but also among species and higher taxonomic units. We first implicate organizational maternal effects of androgens in shaping individual differences in aggressive behaviour emitted by female spotted hyaenas throughout the lifespan. We then compare carnivores and primates with respect to their locomotor and craniofacial adaptations. We inquire whether antagonistic selection pressures on the skull might impose differential functional constraints on evolvability of skulls and brains in these two orders, thus ultimately affecting behavioural flexibility in each group. We suggest that, even when carnivores and primates would theoretically benefit from the same adaptations with respect to behavioural flexibility, carnivores may nevertheless exhibit less behavioural flexibility than primates because of constraints imposed by past adaptations in the morphology of the limbs and skull. Phylogenetic analysis consistent with this idea suggests greater evolutionary lability in relative brain size within families of primates than carnivores. Thus, consideration of developmental constraints may help elucidate variation in mammalian behavioural flexibility.
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