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Generalization during aversive decision-making allows us to avoid a broad range of potential threats following experience with a limited set of exemplars. However, over-generalization, resulting in excessive and inappropriate avoidance, has been implicated in a variety of psychological disorders. Here, we use reinforcement learning modelling to dissect out different contributions to the generalization of instrumental avoidance in two groups of human volunteers (N = 26, N = 482). We found that generalization of avoidance could be parsed into perceptual and value-based processes, and further, that value-based generalization could be subdivided into that relating to aversive and neutral feedback - with corresponding circuits including primary sensory cortex, anterior insula, amygdala and ventromedial prefrontal cortex. Further, generalization from aversive, but not neutral, feedback was associated with self-reported anxiety and intrusive thoughts. These results reveal a set of distinct mechanisms that mediate generalization in avoidance learning, and show how specific individual differences within them can yield anxiety.
Adaptive functioning is thought to reflect a balance between approach and avoidance neural systems with imbalances often producing pathological forms of avoidance. Yet little evidence is available in healthy adults demonstrating a balance between approach and avoidance neural systems and modulation in avoidance neurocircuitry by vulnerability factors for avoidance. Consequently, we used functional magnetic resonance imaging (fMRI) to compare changes in brain activation associated with human avoidance and approach learning and modulation of avoidance neurocircuitry by experiential avoidance. fMRI tracked trial-by-trial increases in activation while adults learned through trial and error an avoidance response that prevented money loss and an approach response that produced money gain. Avoidance and approach cues elicited similar experience-dependent increases in activation in a fronto-limbic-striatal network. Positive and negative reinforcing outcomes (i.e., money gain and avoidance of loss) also elicited similar increases in activation in frontal and striatal regions. Finally, increased experiential avoidance and self-punishment coping was associated with decreased activation in medial/superior frontal regions, anterior cingulate, amygdala and hippocampus. These findings suggest avoidance and approach learning recruit a similar fronto-limbic-striatal network in healthy adults. Increased experiential avoidance also appears to be associated with reduced frontal and limbic reactivity in avoidance, establishing an important link between maladaptive avoidance coping and altered responses in avoidance neurocircuitry.
Background: While there is good evidence that reward learning is underpinned by two distinct decision control systems - a cognitive 'model-based' and a habitbased 'model-free' system, a comparable distinction for punishment avoidance has been much less clear. Methods: We implemented a pain avoidance task that placed differential emphasis on putative model-based and model-free processing, mirroring a paradigm and modelling approach recently developed for reward-based decision-making. Subjects performed a two-step decision-making task with probabilistic pain outcomes of different quantities. The delivery of outcomes was sometimes contingent on a rule signalled at the beginning of each trial, emulating a form of outcome devaluation. Results: The behavioural data showed that subjects tended to use a mixed strategy - favouring the simpler model-free learning strategy when outcomes did not depend on the rule, and favouring a model-based when they did. Furthermore, the data were well described by a dynamic transition model between the two controllers. When compared with data from a reward-based task (albeit tested in the context of the scanner), we observed that avoidance involved a significantly greater tendency for subjects to switch between model-free and model-based systems in the face of changes in uncertainty. Conclusion: Our study suggests a dual-system model of pain avoidance, similar to but possibly more dynamically flexible than reward-based decision-making.
In humans and animals cognitive training during childhood plays an important role in shaping neural circuits and thereby determines learning capacity later in life. Using a negative feedback learning paradigm, the two-way active avoidance (TWA) learning, we aimed to investigate in mice (i) the age-dependency of TWA learning, (ii) the consequences of pretraining in childhood on adult learning capacity and (iii) the impact of sex on the learning paradigm in mice. Taken together, we show here for the first time that the beneficial or detrimental outcome of pretraining in childhood depends on the age during which TWA training is encountered, indicating that different, age-dependent long-term "memory traces" might be formed, which are recruited during adult TWA training and thereby either facilitate or impair adult TWA learning. While pretraining during infancy results in learning impairment in adulthood, pretraining in late adolescence improved avoidance learning. The experiments revealed a clear sex difference in the group of late-adolescent mice: female mice showed better avoidance learning during late adolescence compared to males, and the beneficial impact of late-adolescent pretraining on adult learning was more pronounced in females compared to males.
Serious and debilitating symptoms of anxiety are the most common mental health problem worldwide, accounting for around 5% of all adult years lived with disability in the developed world. Avoidance behavior-avoiding social situations for fear of embarrassment, for instance-is a core feature of such anxiety. However, as for many other psychiatric symptoms the biological mechanisms underlying avoidance remain unclear.
Conditioned place avoidance assays are broadly used in mammals to study different cognitive aspects of operant learning. Here, we introduce a series of experimental designs for training juvenile zebrafish in short-term and long-term conditioned place avoidance assays. Our goal is to promote standardization of animal handling procedures and setup conditions to improve animal welfare and reproducibility while studying operant learning behaviors in juvenile zebrafish. For complete details on the use and execution of this protocol, please refer to Palumbo et al. (2020).
The hippocampus has been implicated in anxiety disorders and post-traumatic stress disorder (PTSD); human studies suggest that a dysfunctional hippocampus may be a vulnerability factor for the development of PTSD. In the current study, we examined the effect of hippocampal damage in avoidance learning, as avoidance is a core symptom of all anxiety disorders. First, the effect of hippocampal damage on avoidance learning was investigated in outbred Sprague Dawley (SD) rats. Second, the function of the hippocampus in Wistar-Kyoto (WKY) rats was compared to SD rats. The WKY rat is an animal model of behavioral inhibition, a risk factor for anxiety, and demonstrates abnormal avoidance learning, marked by facilitated avoidance acquisition and resistance to extinction. The results of the current study indicate that hippocampal damage in SD rats leads to impaired extinction of avoidance learning similar to WKY rats. Furthermore, WKY rats have reduced hippocampal volume and impaired hippocampal synaptic plasticity as compared to SD rats. These results suggest that hippocampal dysfunction enhances the development of persistent avoidance responding and, thus, may confer vulnerability to the development of anxiety disorders and PTSD.
The present study examined the memory modulatory effect of epinephrine on latent learning of an inhibitory avoidance task. Male Sprague-Dawley rats on the first day were subjected to one of three conditions (no, short or long) in pre-exposure to the task apparatus. One day or several days later, they received the typical inhibitory avoidance training with a 0.5 mA/0.5 s foot shock. Memory of the inhibitory avoidance response was tested one day after the foot-shock training. The long pre-exposure group showed better memory than the no or short pre-exposure group, and this latent memory could last for 6 days: Retention scores of the long pre-exposure group were significantly better than those of the no pre-exposure group if the shock training was given 3 or 6 days, but not 12 or 21 days, after the pre-exposure. Epinephrine injected after the pre-exposure training modulated the latent memory in a dose- and time-dependent manner: 0.01 mg/kg given shortly after the short pre-exposure enhanced the memory, but 0.5 mg/kg given shortly after the long pre-exposure impaired it. Epinephrine injected 4 h after the pre-exposure had no effect, neither did that given to rats pre-exposed to a different context. Epinephrine (0.01 mg/kg) also made the latent memory lasting longer as the rats treated with it showed significant avoidance behavior when they had the shock training at 12 or 21 days after the pre-exposure. These findings suggest that epinephrine could modulate memory formed in the latent learning.
Studies have shown that Doxepin has anti-inflammatory effects and reduces oxidative stress. Due to the fact that other tricyclic antidepressants have been shown to have neuroprotective effects, this study aimed to investigate the effects of different doses of doxepin on passive avoidance learning in rats.
Neurological disorders are often accompanied by impairment of memory, attention deficit that cause learning difficulties. Better understanding of learning problems in neurological patients might help to improve the quality of their life. Here we studied the character of fear-based associative learning using the standard active avoidance test in WAG/Rij rats with genetic predisposition to absence epilepsy. Electroencephalographic properties of spike-wave seizures (i.e., hallmarks of absence epilepsy) were examined at the age of 5 and 7 m. Around 24 % of rats did not express epileptic activity despite genetic predisposition. In the active avoidance test, 6 m old rats with the epileptic phenotype needed more trails to obtain the first avoidance than non-epileptic rats, but showed the same number of avoidances to reach the learning criterion. The total time of spike-wave activity positively correlated with the outcomes of avoidance performance only in subjects with severe epilepsy, but not in subjects with mild epilepsy. In order to evaluate early sensory (epigenetic) factors governing cognitive comorbidities in adult WAG/Rij rats, we performed bilateral whisker trimming during PN1-8 and PN9-16. This led to a quicker development of SWD, but did not influence cognitive abilities at the age of 6 m. In summary, epileptic WAG/Rij rats had difficulties with executive functions before the first avoidance of adverse stimulus, rather than impairment of memory after the first avoidance. Our data assume that cognitive comorbidities in epileptic WAG/Rij rats primarily may relate to executive deficit during the initial stage of avoidance test and secondary - to impairment of short-term memory. This fits well to outcomes of clinical studies in patients with generalized epilepsy.
Individuals with psychopathy often show deficits in learning, which often have negative consequences. Several theories have been proposed to explain psychopathic behaviors, but the learning mechanisms in psychopathy are still unclear. To clarify the learning anomalies in psychopathy, we fitted reinforcement learning (RL) models to behavioral data. We conducted two experiments to examine the effect of psychopathy as a group difference (Experiment 1) and as a continuum (Experiment 2). Forty-three undergraduates (in Experiment 1) and fifty-five undergraduate and graduate students (in Experiment 2) performed a go/no-go based learning task with accompanying rewards or punishments. Although we observed no differences in learning performance among the levels of psychopathic traits, the learning rate for the positive prediction error in the loss domain was lower for those with high-psychopathic trait than for those with low-psychopathic trait. This finding indicates that individuals with high-psychopathic traits update an action value less when they avoid a negative outcome. Our model can represent previous theories under a computational framework and provide a new perspective on impaired learning in psychopathy.
The avoidance of starvation is critical for the survival of most organisms, thus animals change behavior based on past nutritional conditions. Insulin signaling is important for nutritional state-dependent behavioral plasticity, yet the underlying regulatory mechanism at the cellular level remains unclear. Previous studies showed that insulin-like signaling is required for taste avoidance learning, in which the nematode Caenorhabditis elegans avoids salt concentrations encountered under starvation conditions. DAF-2c, a splice isoform of the DAF-2 insulin receptor, functions in the axon of the ASER sensory neuron, which senses changes in salt concentrations. In addition, mutants of a major downstream factor of DAF-2, the forkhead transcription factor O (FOXO) homolog DAF-16, show defects in taste avoidance learning. Interestingly, the defect of the daf-2 mutant is not suppressed by daf-16 mutations in the learning, unlike those in other phenomena, such as longevity and development. Here we show that multiple DAF-16 isoforms function in ASER. By epistasis analysis using a DAF-2c isoform-specific mutant and an activated form of DAF-16, we found that DAF-16 acts in the nucleus in parallel with the DAF-2c-dependent pathway in the axon, indicating that insulin-like signaling acts both in the cell body and axon of a single neuron, ASER. Starvation conditioning induces nuclear translocation of DAF-16 in ASER and degradation of DAF-16 before starvation conditioning causes defects in taste avoidance learning. Forced nuclear localization of DAF-16 in ASER biased chemotaxis towards lower salt concentrtions and this effect required the Gq/PKC pathway and neuropeptide processing enzymes. These data imply that DAF-16/FOXO transmits starvation signals and modulates neuropeptide transmission in the learning.
It is challenging to avoid obstacles safely and efficiently for multiple robots of different shapes in distributed and communication-free scenarios, where robots do not communicate with each other and only sense other robots' positions and obstacles around them. Most existing multi-robot collision avoidance systems either require communication between robots or require expensive movement data of other robots, like velocities, accelerations and paths. In this paper, we propose a map-based deep reinforcement learning approach for multi-robot collision avoidance in a distributed and communication-free environment. We use the egocentric local grid map of a robot to represent the environmental information around it including its shape and observable appearances of other robots and obstacles, which can be easily generated by using multiple sensors or sensor fusion. Then we apply the distributed proximal policy optimization (DPPO) algorithm to train a convolutional neural network that directly maps three frames of egocentric local grid maps and the robot's relative local goal positions into low-level robot control commands. Compared to other methods, the map-based approach is more robust to noisy sensor data, does not require robots' movement data and considers sizes and shapes of related robots, which make it to be more efficient and easier to be deployed to real robots. We first train the neural network in a specified simulator of multiple mobile robots using DPPO, where a multi-stage curriculum learning strategy for multiple scenarios is used to improve the performance. Then we deploy the trained model to real robots to perform collision avoidance in their navigation without tedious parameter tuning. We evaluate the approach with multiple scenarios both in the simulator and on four differential-drive mobile robots in the real world. Both qualitative and quantitative experiments show that our approach is efficient and outperforms existing DRL-based approaches in many indicators. We also conduct ablation studies showing the positive effects of using egocentric grid maps and multi-stage curriculum learning.
The brain is extensively vascularized, useŝ20% of the body's oxygen, and is highly sensitive to changes in oxygen. While synaptic plasticity and memory are impaired in healthy individuals by exposure to mild hypoxia, aged individuals appear to be even more sensitive. Aging is associated with progressive failure in pulmonary and cardiovascular systems, exposing the aged to both chronic and superimposed acute hypoxia. The HIF proteins, the "master regulators" of the cellular response to hypoxia, are robustly expressed in neurons and astrocytes. Astrocytes support neurons and synaptic plasticity via complex metabolic and trophic mechanisms. The activity of HIF proteins in the brain is diminished with aging, and the increased exposure to chronic and acute hypoxia with aging combined with diminished HIF activity may impair synaptic plasticity.
Previous research across species has shown that the amygdala is critical for learning about aversive outcomes, while the striatum is involved in reward-related processing. Less is known, however, about the role of the amygdala and the striatum in learning how to exert control over emotions and avoid negative outcomes. One potential mechanism for active avoidance of stressful situations is postulated to involve amygdala-striatal interactions. The goal of this study was to investigate the physiological and neural correlates underlying avoidance learning in humans. Specifically, we used a classical conditioning paradigm where three different conditioned stimuli (CS) were presented. One stimulus predicted the delivery of a shock upon stimulus offset (CS+), while another predicted no negative consequences (CS-). A third conditioned cue also predicted delivery of a shock, but participants were instructed that upon seeing this stimulus, they could avoid the shock if they chose the correct action (AV+). After successful learning, participants could then easily terminate the shock during subsequent stimulus presentations (AV-). Physiological responses (as measured by skin conductance responses) confirmed a main effect of conditioning, particularly showing higher arousal responses during pre (AV+) compared to post (AV-) learning of an avoidance response. Consistent with animal models, amygdala-striatal interactions were observed to underlie the acquisition of an avoidance response. These results support a mechanism of active coping with conditioned fear that allows for the control over emotional responses such as fears that can become maladaptive and influence our decision-making.
Stress can alter response to nociception. Under certain circumstances stress enhances nociception, a phenomenon which is called stress-induced hyperalgesia (SIH). While nociception has been studied in this paradigm, possible alterations occurring in passive avoidance (PA) learning after exposing rats to this type of stress has not been studied before.
In reforested areas, underground strychnine baiting to control pocket gophers (Thomomys mazama) poses a hazard to golden mantled ground squirrels (Spermophilus lateralis) and yellow pine chipmunks (Eutamias amoenus). We designed this study to assess whether: 1) chemical insensitivity to bitter tastes might explain the ingestion of strychnine; 2) pocket gophers would avoid four bitter-tasting compounds: quebracho (QUEB), sucrose octaacetate (SOA), quinine hydrochloride (QHCl), and denatonium benzoate (DB); and 3) nontarget species could be trained to avoid strychnine paired with the most aversive compound. Our results showed that while all species readily consumed strychnine, the nontarget species could be conditioned to avoid it. Moreover, while high (0.1%) concentrations of DB, quinine hydrochloride, and quebracho reduced consumption by pocket gophers, 0.05% DB was inoffensive. Nontarget animals readily avoided 0.05% DB, and avoidance was stronger after conditioning. Together, our results suggest that all of the rodents tested are insensitive to strychnine, high concentrations of some bitter tastes may be effective pocket gopher repellents, and lower concentrations of DB may selectively repel nontarget animals from strychnine baits.
Alzheimer's disease was known as a progressive neurodegenerative disorder in the elderly and is characterized by dementia and severe neuronal loss in the some regions of brain such as nucleus basalis magnocellularis. It plays an important role in the brain functions such as learning and memory. Loss of cholinergic neurons of nucleus basalis magnocellularis by ibotenic acid can commonly be regarded as a suitable model of Alzheimer's disease. Previous studies reported that exercise training may slow down the onset and progression of memory deficit in neurodegenerative disorders. This research investigates the effects of treadmill running on acquisition and retention time of passive avoidance deficits induced by ibotenic acid nucleus basalis magnocellularis lesion.
A one-trial learning task, where chicks learn that a bead of a particular shape and/or colour has a bitter taste (because it has been coated in 100% methyl anthranilate, MeA) and subsequently avoids it on test, has been widely used by research groups across the world. However, there are some differences in the results reported by different research laboratories. One important difference is found when chicks are trained with a diluted bitter taste on the bead (10 or 20% MeA); memory is not consolidated and fades, lasting for different times. At Monash and La Trobe Universities, memory lasts for 30 min but at the Open University (OU), memory lasts for 4-6h before fading. Differences in protocol that may explain this apparent discrepancy are whether the chicks have seen the bead before (novelty) and whether the colour or the shape of the bead is an important feature. In this review, we discuss these and other factors that may contribute to the differences in the characteristics of memory processing at Monash and at the OU, such as chick strain, hatchery or laboratory incubated chicks, age at training. It is clear that there is a difference between passive avoidance and discriminative avoidance protocols and this may explain the differences in duration of the memory with weakly reinforced learning. Is the OU task a more salient experience because of the novelty of the bead and therefore a 'stronger' learning experience? The different protocols may allow different questions to be addressed.
Avoidance behavior is a typically adaptive response performed by an organism to avert harmful situations. Individuals differ remarkably in their tendency to acquire and perform new avoidance behaviors, as seen in anxiety disorders where avoidance becomes pervasive and inappropriate. In rodent models of avoidance, the inbred Wistar-Kyoto (WKY) rat demonstrates increased learning and expression of avoidance compared to the outbred Sprague Dawley (SD) rat. However, underlying mechanisms that contribute to these differences are unclear. Computational modeling techniques can help identify factors that may not be easily decipherable from behavioral data alone. Here, we utilize a reinforcement learning (RL) model approach to better understand strain differences in avoidance behavior. An actor-critic model, with separate learning rates for action selection (in the actor) and state evaluation (in the critic), was applied to individual data of avoidance acquisition from a large cohort of WKY and SD rats. Latent parameters were extracted, such as learning rate and subjective reinforcement value of foot shock, that were then compared across groups. The RL model was able to accurately represent WKY and SD avoidance behavior, demonstrating that the model could simulate individual performance. The model determined that the perceived negative value of foot shock was significantly higher in WKY than SD rats, whereas learning rate in the actor was lower in WKY than SD rats. These findings demonstrate the utility of computational modeling in identifying underlying processes that could promote strain differences in behavioral performance.
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