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Yawning is a stereotypical behavior pattern commonly associated with other behaviors such as grooming, sleepiness, and arousal. Several differences in behavioral and neurochemical characteristics have been described in high-yawning (HY) and low-yawning (LY) sublines from Sprague-Dawley (SD) rats that support they had changes in the neural mechanism between sublines. Differences in behavior and neurochemistry observed in yawning sublines could also overlap in processes needed during taste learning, particularly during conditioned taste aversion (CTA) and its latent inhibition. Therefore, the aim of this study was to analyze taste memory differences, after familiarization to novel or highly sweet stimuli, between yawning sublines and compare them with outbred SD rats. First, we evaluated changes in appetitive response during long-term sugar consumption for 14 days. Then, we evaluated the latent inhibition of CTA strength induced by this long pre-exposure, and we also measured aversive memory extinction rate. The results showed that SD rats and the two sublines developed similar CTA for novel sugar and significantly stronger appetitive memory after long-term sugar exposure. However, after 14 days of sugar exposure, HY and LY sublines were unable to develop latent inhibition of CTA after two acquisition trials and had a slower aversive memory extinction rate than outbreed rats. Thus, the inability of the HY and LY sublines to develop latent inhibition of CTA after long-term sugar exposure could be related to the time/context processes involved in long-term appetitive re-learning, and in the strong inbreeding that characterizes the behavioral traits of these sublines, suggesting that inbreeding affects associative learning, particularly after long-term exposure to sweet stimuli which reflects high familiarization.

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Morphine administered shortly after exposure to a novel environment induces potent locomotor stimulant conditioning. Environmental novelty is important as pre-exposure (PE) to a stimulus can attenuate the capacity to acquire conditioned stimulus (CS). Here, the importance of environmental novelty for the efficacy of an open-field to become a CS for elicitation of a morphine conditioned response was assessed by comparing the effects of morphine administered post-trial following a 5 min exposure to a novel environment versus a PE environment. Four groups of rats (2 vehicle and 2 morphine groups) were used. Two groups received ten daily 5 min non-drug PEs to an open-field arena and the other two groups were not pre-exposed to the environment. Subsequently, all groups received post-trial injections of either vehicle or morphine immediately after each of five daily 5 min sessions in the open-field. Importantly, on the first day of testing prior to the first post-test morphine administration, the locomotor activity of the novel and PE groups was not different. Over the 5 post-trial morphine treatments, the activity of the PE morphine group, the PE vehicle and the novel environment vehicle groups did not change and were equivalent. In contrast, in the novel environment morphine group, a conditioned hyper-activity response increased with repeated post-trial morphine treatments. For the morphine group it is suggested that the novel environment initiated a post-trial stimulus trace that occurred in temporal contiguity with the post-trial drug response and enabled the trace to become a CS for the morphine unconditioned response. In contrast, PE induced a latent inhibition effect in the PE morphine group, thus the post-trial CS trace was insufficient to become associated to the morphine response and no conditioning occurred. In addition to conventional drug induced Pavlovian delay conditioning, the findings are suggestive of drug induced Pavlovian trace conditioning.

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Benzodiazepines are usually prescribed for anxiety and sleep disorders in long-term schedules that may cause drug dependence. Discontinuation after prolonged administration may lead to withdrawal expression, being anxiety the most predominant sign. The context-dependent associative learning process that underlies diazepam dependence can be interfered by pre-exposure to the drug administration context, an effect known as latent inhibition. Considering this background, the primary aim of the present investigation is to develop a therapeutic strategy to prevent diazepam withdrawal in male Wistar rats by interfering with this learning process. Nitric oxide is a crucial player in learning and memory, hippocampal synaptic transmission and in diazepam withdrawal. Then, a secondary goal is to determine how latent inhibition could alter functional plasticity and neuronal nitric oxide synthase enzyme (NOS-1) expression within the hippocampus, by using multi-unitary cell recordings and Western blot, respectively. Our results indicate that chronic diazepam treated animals under latent inhibition did not show anxiety, or changes in hippocampal synaptic transmission, but a significant reduction in NOS-1 expression was observed. Accordingly, pharmacological NOS-1 inhibition resembles behavioral and electrophysiological changes induced by latent inhibition. Contrary, diazepam treated animals under Control protocol expressed anxiety and evidenced an increased hippocampal-plasticity, without alterations in NOS-1 expression. In conclusion, manipulation of the contextual cues presented during diazepam administration may be considered as an effective non-pharmacological tool to prevent the withdrawal syndrome. This behavioral strategy may influence hippocampal synaptic transmission, probably by alterations in nitric oxide signaling pathways in this structure.

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The medial prefrontal cortex (mPFC) has reciprocal projections with many cerebral structures that are crucial in the control of food ingestion behavior and reward processing; Thus the mPFC has an important function in taste memory recognition. Previous results indicate that long-term consumption of sugar produces changes in appetitive re-learning and suggest that this could trigger an escalating consumption due to the inability to learn new negative consequences related to the same taste. Further evidence suggests that general identity reward value could be encoded in the mPFC. Therefore, the purpose of this study was to evaluate in rats whether after 21 days of sugar consumption the increase in sweet taste preference and latent inhibition of conditioned taste aversion (CTA) were affected differentially by pharmacological activation or blockage of dopaminergic and ß-adrenergic receptors, in the mPFC, during CTA acquisition. Results showed that after long-term sugar exposure, mPFC activation of ß-adrenergic receptors with clenbuterol delayed aversive memory extinction, but the blockade with propranolol or activation of dopaminergic receptors with apomorphine increased CTA latent inhibition and accelerated aversive memory extinction only after acute sugar exposure. Only dopaminergic blockade with haloperidol prevented sweet taste preference expression after long-term sugar consumption, increased CTA latent inhibition and accelerated extinction after acute sugar exposure. Taken together, the present data provide evidence that catecholaminergic receptors in the mPFC after prolonged sugar consumption underwent functional changes related to re-learning and new aversive taste learning.

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Learning about olfactory stimuli is essential in bumblebees' life since it is involved in orientation, recognition of nest sites, foraging efficiency and food yield for the colony as a whole. To evaluate associative learning abilities in bees under controlled environmental conditions, the proboscis extension response (PER) assay is a well-established method used in honey bees, stingless bees and successfully adapted to bumblebees of the genus Bombus. However, studies on the learning capacity of Bombus atratus (Hymenoptera: Apidae), one of the most abundant native species in South America, are non-existent. In this study, we examined the cognitive abilities of worker bees of this species, carrying out an olfactory PER conditioning experiment. Bumblebees were able to learn a pure odor when it was presented in paired association with sugared reward, but not when odor and reward were presented in an unpaired manner. Furthermore, if the bees were preexposed to the conditioned odor, the results differed depending on the presence of the scent either as a volatile in the rearing environment or diluted in the food. A decrement in learning performance results from the non-reinforced pre-exposure to the to-be-conditioned odor, showing a latent inhibition phenomenon. However, if the conditioned odor has been previously offered diluted in sugared reward, the food odor acts as a stimulus that improves the learning performance during PER conditioning. The native bumblebee B. atratus is thus a new hymenopteran species capable of being trained under controlled experimental conditions. Since it is an insect increasingly reared for pollination service, this knowledge could be useful in its management in crops.

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En este artículo se describen desde una perspectiva comparativa los fenómenos de bloqueo, ensombrecimiento e inhibición latente, enfatizando su presencia en tareas de aprendizaje espacial. Estos fenómenos de aprendizaje, ampliamente observados en otras clases de vertebrados e invertebrados, han sido recientemente descriptos por primera vez en anfibios, un grupo de vertebrados con un cerebro filogenéticamente antiguo. Tomando como modelo al sapo terrestre Rhinella arenarum, se revisarán los tres fenómenos de aprendizaje asociativo mencionados en una situación de aprendizaje espacial: (1) bloqueo entre claves visuales asociadas a una meta, (2) ensombrecimiento de una clave visual lejana por la presencia de una clave cercana y (3) inhibición latente debida a la pre-exposición a una clave visual. Todos los entrenamientos se llevaron a cabo en una arena circular de color blanco, utilizando agua como recompensa. Dentro de la arena, se distribuyeron cuatro piletas de acrílico en forma de cruz contra las paredes laterales (sólo una tenía acceso a la recompensa). En las paredes interiores de la arena circular se colocaron varias señales visuales para guiar a los animales. Los resultados obtenidos en sapos indican que estos fenómenos, observados previamente en aves y mamíferos, también se encuentran en este grupo (utilizando un paradigma de aprendizaje espacial con claves visuales cercanas y lejanas). Este primer registro en anfibios sugiere que los mecanismos biológicos de estos fenómenos de aprendizaje han surgido muy tempranamente en el curso de la evolución de los vertebrados totalmente terrestres y que los mismos han sido fuertemente conservados. El análisis comparado de estos hallazgos contribuirá a mejorar el entendimiento de los mecanismos biológicos que subyacen al aprendizaje espacial, en busca de patrones funcionales comunes con otras clases de vertebrados y potencialmente presentes en un ancestro común.

This article describes blocking, overshadowing and latent inhibition phenomena from a comparative perspective, emphasizing their presence in spatial learning tasks. These learning phenomena, previously observed in other vertebrates and invertebrates classes, have been recently reported for the first time in amphibians, a vertebrate group with a phylogenetically ancient brain. We use the terrestrial toad Rhinella arenarum as animal model to analyze the three mentioned associative phenomena in a spatial learning situation: (1) blocking between visual cues associated to a goal, (2) overshadowing of a distant visual cue by the presence of a nearby cue, and (3) latent inhibition generated by the pre-exposure to a visual cue. All trainings were conducted in a white circular arena, using water as reward. Inside the arena, four green acrylic container were distributed in a cross shape against the side walls (only one with access to reward). On the inner walls of the circular arena they were placed several visual cues for guiding animals. In all studies described in this article toads were partially dehydrated to motivate them to search for water. In the blocking situation, experimental animals had the rewarded container signaled by a visual cue on the wall above the container. In the second phase of training other visual cue was added. The results revealed that in these animals the prior training with only one of the visual cues blocked the association of the reward with the other cue, when both cues were then presented simultaneously to indicate the position of reward. In the overshadowing situation, experimental animals had from the beginning the rewarded container signaled by two visual cues on the wall, one to 10 cm right (named near cue), and the other placed approximately 70 cm to the left (between the adjacent pool and the opposite, named far cue). The results indicated that the location of a visual cue located away from reward was overshadowed by the presence of a nearby cue. Finally, in the situation of latent inhibition, animals of pre-exposed group had five previous training sessions, where a visual cue was presented without reward. Then, when in the subsequent training this visual cue signaled the reward, animals pre-exposed needed more sessions to reach the asymptote of learning compared to other non-pre-exposed animals. Therefore, the pre-exposure to the visual cue (i.e., unreinforced exposure to the stimulus) significantly retarded the acquisition, delaying the association of this cue with the reward. Taking into account that these phenomena have been observed previously in birds and mammals, this first record in amphibians (using a spatial learning paradigm with near and far visual cues) suggests that biological mechanisms of these learning phenomena have emerged very early in the course of the evolution of fully terrestrial vertebrates and that they have been strongly preserved. With regard to the underlying neural substrates, the relationship of the hippocampal formation with the processes of learning and spatial memory is a constant in all vertebrate species studied. Analyzing the particular case of amphibians, compared with other groups of tetrapods, their telencephalon has a simple organization (in the evolutionary sense non-derived). In this aspect, the medial pallium, region in the dorso-medial quadrant of the hemisphere, is considered homologous to the mammalian hippocampal formation (based on their topographic position, its interconnections with other telencephalic areas and neurohistochemical data). Heretofore, the dependence of spatial learning with the functioning of the medial cortex was thought to be a primitive character of amniotes. However, this feature can now be extended to the group of amphibians, as recently has been observed that the lesion of the medial pallium impairs spatial learning. Thus, the evidence collected until this moment in amphibians suggests that this relationship may have emerged earlier than previously thought. On the whole, the comparative analysis of these findings will contribute to a better understanding of the biological mechanisms underlying spatial learning, thereby looking for common functional patterns with other vertebrate classes, potentially present in a common ancestor.

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Preexposure to a conditioned stimulus (CS) usually weakens conditioning, an effect known as latent inhibition. Similar to other learning interference effects, latent inhibition has been characterized as context-dependent, which means that the magnitude of this effect can be attenuated by changing the context between the different phases of the procedure (e.g., preexposure and conditioning). Latent inhibition has been found with a variety of procedures in infant rats, but the few studies that examined the context-dependency of this phenomenon during this ontogenetic period found no context-change effect. The present study explored the context-dependency of latent inhibition during infancy using a conditioned taste aversion preparation and employing contexts enriched with distinctive odors to increase the possible efficacy of the context manipulation. Experiment 1 showed that three preexposures to the CS (saccharin) were sufficient to retard conditioning to the same CS, although this effect was also observed in a control group preexposed to an alternative taste stimulus (saline), in comparison with a non-preexposed control group. In Experiment 2a, the CS-preexposure effect was found to be specific to the preexposed CS when the number of preexposures was increased. This effect was revealed as context-dependent in Experiment 2b, since it was attenuated by changing the context between preexposure and conditioning. The present result is consistent with recent studies showing the context-dependency of extinction in preweanling rats, thus demonstrating these animals' capacity to learn about context early on in their development.

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