Temporary basolateral amygdala lesions disrupt acquisition of socially transmitted food preferences in rats

Lesions of the basolateral amygdala (BLA) have long been associated with abnormalities of taste-related behaviors and with failure in a variety of taste- and odor-related learning paradigms, including taste-potentiated odor aversion, conditioned taste preference, and conditioned taste aversion. Still, the general role of the amygdala in chemosensory learning remains somewhat controversial. In particular, it has been suggested that the amygdala may not be involved in a form of chemosensory learning that has recently received a substantial amount of study-socially transmitted food preference (STFP). Here, we provide evidence for this involvement by pharmacologically inactivating the basolateral amygdala bilaterally during STFP training. The same inactivation sites that impaired taste aversion learning eliminated the normally conditioned preference for a food smelled on a conspecific's breath. Impairments of learned preference persisted even in testing sessions in which BLA was not inactivated, and learning was normal when the BLA was inactivated only during testing sessions; thus, the impairment was a true acquisition deficit. In conjunction with previous results from other paradigms, therefore, our data suggest that the amygdala is vital for learning procedures involving pairings of potent and arbitrary chemosensory stimuli.     

Time of day modulation of conditioned place preference in rats depends on the strain of rat used

In golden hamsters, the expression of a conditioned place preference (CPP) or avoidance (CPA) is regulated in a circadian pattern such that the preference and avoidance are exhibited strongly at the circadian time of prior training, but not at other circadian times. In the rat, reports are conflicting regarding whether time of day learning is evident. We investigated whether this conflict arises because different strains of rat have been used. In this experiment, Long Evans and Wistar rats were trained at a specific circadian time to discriminate between a context paired with food reward and an unpaired context. Animals were then tested for preference at the same or a different circadian time. Long Evans rats showed preference for the paired context at both times tested, whereas Wistar rats showed preference only when training and testing times matched. The results show that time of day learning can be generalized to rats using the Wistar strain.     

Effects of excitotoxic brain lesions on taste-mediated odor learning in the rat

The association learning between taste and odor is important in ingestive behavior. For a better understanding of this learning, we have developed a convenient and useful paradigm to assess the taste-mediated odor learning. In the training session, Wistar male rats drank water from two bottles in their home cages and from eight small glass dishes. In the learning session they were exposed in their home cages and also in a circular open-field apparatus to 0.005 M Na-saccharin and 0.02 M quinine hydrochloride which contained either banana or almond odors. One learning trial consisted of this pair of exposures. The preceding behavioral experiment has shown that these two odors are not aversive and are differentially perceived by rats. In the test session, the animals were put in the open-field apparatus equipped with eight dishes: four contained water with banana, and another four, with almond. Normal control rats preferred to drink water with the odor previously associated with saccharin. Stronger and more persistent preference was attained after two or three learning trials. To elucidate the brain sites responsible for this taste-mediated odor learning, the same procedure was assessed on brain-lesioned rats. Rats with lesions in the amygdala showed rapid extinction of preference to the saccharin-associated odor, whereas control rats did not. However, rats with lesions in the insular cortex showed retention of learning similar to that of the control rats. Rats with lesions in the sulcal prefrontal or cingulate cortices showed moderate disruptive effects on preference to the saccharin-associated odor. In conclusion, the odor learning established in our experimental paradigm is based on the association between the quality of odor and hedonics of taste. The amygdala may play a role in the formation, at least in the retention process, of this taste-odor association learning.     

Floral guidance of learning a preference for symmetry by bumblebees

This study examines the mechanism underlying one way in which bumblebees are known to develop a preference for symmetric patterns: through prior non-differential reinforcement on simple patterns (black discs and white discs). In three experiments, bees were given a choice among symmetric and asymmetric black-and-white non-rewarding patterns presented at the ends of corridors in a radial maze. Experimental groups had prior rewarded non-discrimination training on white patterns and black patterns, while control groups had no pre-test experience outside the colony. No preference for symmetry was obtained for any of the control groups. Prior training with circular patterns highlighting a horizontal axis of symmetry led to a specific subsequent preference for horizontal over vertical symmetry, while training with a vertical axis abolished this effect. Circles highlighting both axes created a general avoidance of asymmetry in favour of symmetric patterns with vertical, horizontal or both axes of symmetry. Training with plain circles, but not with deformed circles, led to a preference for symmetry: there was no evidence that the preference emerged just by virtue of having attention drawn away from irrelevant pattern differences. Our results point to a preference for symmetry developing gradually through first learning to extract an axis of symmetry from simple patterns and subsequently recognizing that axis in new patterns. They highlight the importance of continued learning through non-differential reinforcement by skilled foragers. Floral guides can function not only to guide pollinators to the source of reward but also to highlight an axis of symmetry for use in subsequent floral encounters.     

Computer-based training versus traditional lecture: Effect on learning and retention

This study investigated the effectiveness of computer-based training (CBT) versus the standard or traditional lecture method. The study was conducted at a large pharmaceutical manufacturing site located in Eastern North Carolina. Subjects were chemical processors in the bulk chemical production division (N=54). All subjects completed a comprehensive hazardous chemicals safety training program, with one treatment group completing the course via a self-directed computer program (n=27) and one completing the course via traditional instructor-led sessions (n=27). Both delivery formats were identical relative to learning objectives and content. Level of learning was assessed via a 33-item pretest and posttest. Subjects were also administered a 33-item retention test one month following completion of the program. Subject biographical data, including educational level, were collected by questionnaire and the Computer Anxiety Index (CAIN) was administered to assess subjects' level of computer anxiety within the CBT group. Satisfaction with training was assessed in both treatment groups. Results indicated 1) both groups demonstrated significant learning following training, 2) there was no significant difference in level of learning between the two groups, 3) retention after one month was significantly higher in the CBT groups, 4) there was no correlation between educational level or computer anxiety and learning, and 5) there was no significant difference between the two groups on satisfaction with the training experience.     

Spatial and reversal learning in the Morris water maze are largely resistant to six hours of REM sleep deprivation following training

This first test of the role of REM (rapid eye movement) sleep in reversal spatial learning is also the first attempt to replicate a much cited pair of papers reporting that REM sleep deprivation impairs the consolidation of initial spatial learning in the Morris water maze. We hypothesized that REM sleep deprivation following training would impair both hippocampus-dependent spatial learning and learning a new target location within a familiar environment: reversal learning. A 6-d protocol was divided into the initial spatial learning phase (3.5 d) immediately followed by the reversal phase (2.5 d). During the 6 h following four or 12 training trials/day of initial or reversal learning phases, REM sleep was eliminated and non-REM sleep left intact using the multiple inverted flowerpot method. Contrary to our hypotheses, REM sleep deprivation during four or 12 trials/day of initial spatial or reversal learning did not affect training performance. However, some probe trial measures indicated REM sleep-deprivation-associated impairment in initial spatial learning with four trials/day and enhancement of subsequent reversal learning. In naive animals, REM sleep deprivation during normal initial spatial learning was followed by a lack of preference for the subsequent reversal platform location during the probe. Our findings contradict reports that REM sleep is essential for spatial learning in the Morris water maze and newly reveal that short periods of REM sleep deprivation do not impair concurrent reversal learning. Effects on subsequent reversal learning are consistent with the idea that REM sleep serves the consolidation of incompletely learned items.     

Inhibition of nitric oxide synthase impairs early olfactory associative learning in newborn rats

The present experiments examined the role of nitric oxide ( NO) in early associative olfactory learning in rats. A preference for peppermint odor was induced by pairing peppermint odor with tactile stimulation in Wistar rat pups, in either a repetitive training paradigm or in a one-trial olfactory learning paradigm. In a first experiment we studied the effect of nitric oxide synthase (NOs) inhibition on early olfactory learning in a repetitive paradigm, by systemic daily injections of NG-nitro-l-arginine methyl ester (l-NAME, 50 mg/kg, i.p.). In order to exclude possible deleterous effects of repeated injections of l-NAME, we explored in a second experiment the effect of a single inhibitor injection in a one-trial olfactory learning paradigm. Inhibition of NOs was performed by either administration of l-NAME (50 mg/kg, i.p.), or 7-nitroindazole (7-NI, 30 mg/kg, i.p.), a more selective inhibitor of the neuronal NOs. We showed that both l-NAME and 7-NI impaired early olfactory associative learning when given before training but not before subsequent testing. Considering that NOs neurons are already widespread in the central nervous system (the olfactory bulb included) during the first postnatal week, the sites where NO inhibition may have acted to impair olfactory learning are discussed. The mechanisms of action of NO in relation with other neurotransmitters known to be necessary for olfactory conditioning in rat pups remain to be established. Impairment by NO synthesis inhibition of the acquisition during the first postnatal week of an olfactory conditioning, but not its recall, suggests a role for NO at synapses involved in that learning.     

Memory for time of training modulates performance on a place conditioning task in marmosets

In rodents, the expression of a reward-conditioned place preference (CPP) is regulated in a circadian pattern such that the preference is exhibited strongly at the circadian time of prior training but not at other circadian times. Because each animal is trained only at a single circadian phase, the concept of time as a context cue is derived from a rhythmic internal state rather than learned explicitly from the external cues. We now report that the same “time memory” is expressed following context conditioning in the common marmoset (Callithrix jacchus). Animals were trained at a specific time to discriminate between an unpaired context and a context paired with food reward. Marmosets were then tested for preference at circadian times that were either the same or different from the training time. Preference was expressed only when training and testing times matched. The results show that time of day learning can be generalized to this new world primate implying that a similar circadian mechanism might regulate craving for reward in diverse mammals including human beings.     

Odor preference learning and memory modify GluA1 phosphorylation and GluA1 distribution in the neonate rat olfactory bulb: testing the AMPA receptor hypothesis in an appetitive learning model

An increase in synaptic AMPA receptors is hypothesized to mediate learning and memory. AMPA receptor increases have been reported in aversive learning models, although it is not clear if they are seen with memory maintenance. Here we examine AMPA receptor changes in a cAMP/PKA/CREB-dependent appetitive learning model: odor preference learning in the neonate rat. Rat pups were given a single pairing of peppermint and 2 mg/kg isoproterenol, which produces a 24-h, but not a 48-h, peppermint preference in the 7-d-old rat pup. GluA1 PKA-dependent phosphorylation peaked 10 min after the 10-min training trial and returned to baseline within 90 min. At 24 h, GluA1 subunits did not change overall but were significantly increased in synaptoneurosomes, consistent with increased membrane insertion. Immunohistochemistry revealed a significant increase in GluA1 subunits in olfactory bulb glomeruli, the targets of olfactory nerve axons. Glomerular increases were seen at 3 and 24 h after odor exposure in trained pups, but not in control pups. GluA1 increases were not seen as early as 10 min after training and were no longer observed 48 h after training when odor preference is no longer expressed behaviorally. Thus, the pattern of increased GluA1 membrane expression closely follows the memory timeline. Further, blocking GluA1 insertion using an interference peptide derived from the carboxyl tail of the GluA1 subunit inhibited 24 h odor preference memory providing causative support for our hypothesis. PKA-mediated GluA1 phosphorylation and later GluA1 insertion could, conjointly, provide increased AMPA function to support both short-term and long-term appetitive memory.     

A Comparison of Written,Vocal, and Video Feedback When Training Teachers

We compared the effectiveness of and preference for different feedback strategies when training six special education teachers during a 5-day summer training program. In Experiment 1, teachers received written or vocal feedback while learning to implement two different types of preference assessments. In Experiment 2, we compared either written or vocal feedback to vocal feedback combined with video replays of performance while training the teachers to implement two variations of discrete-trial training. The different forms of feedback were similarly effective for all of the participants. However, all of the teachers showed a preference for vocal feedback when they could choose which form of feedback they would receive from the experimenter. Results have important implications for the use of feedback when training teachers.     

Modification of prenatal auditory experience alters postnatal auditory preferences of bobwhite quail chicks.

This study assessed the effects of altered prenatal auditory experience on bobwhite quail chicks' (Colinus virginianus) species-specific preference for the bobwhite maternal call. Results revealed that when the repetition rate of the embryonic vocalizations normally present in the prenatal environment was altered, the species-typical auditory preference of hatchlings for the maternal call was also altered. Specifically, embryos exposed to embryonic vocalizations with a faster repetition rate than normal subsequently preferred a bobwhite maternal call with a faster repetition rate over one with its normal repetition rate. Bobwhite embryos thus appear able to abstract features of their prenatal auditory environment to other auditory events in the postnatal period. This demonstration of prenatal perceptual learning is in keeping with other recent studies from behavioural embryology, which have also demonstrated that prenatal perceptual experience can influence later responses to species-typical stimulation.     

Peak shift in honey bee olfactory learning

If animals are trained with two similar stimuli such that one is rewarding (S+) and one punishing (S?), then following training animals show a greatest preference not for the S+, but for a novel stimulus that is slightly more different from the S? than the S+ is. This peak shift phenomenon has been widely reported for vertebrates and has recently been demonstrated for bumblebees and honey bees. To explore the nature of peak shift in invertebrates further, here we examined the properties of peak shift in honey bees trained in a free-flight olfactory learning assay. Hexanal and heptanol were mixed in different ratios to create a continuum of odour stimuli. Bees were trained to artificial flowers such that one odour mixture was rewarded with 2 molar sucrose (S+), and one punished with distasteful quinine (S?). After training, bees were given a non-rewarded preference test with five different mixtures of hexanal and heptanol. Following training bees’ maximal preference was for an odour mixture slightly more distinct from the S? than the trained S+. This effect was not seen if bees were initially trained with two distinct odours, replicating the classic features of peak shift reported for vertebrates. We propose a conceptual model of how peak shift might occur in honey bees. We argue that peak shift does not require any higher level of processing than the known olfactory learning circuitry of the bee brain and suggest that peak shift is a very general feature of discrimination learning.     

Extinction of Within-event Learning Is Contextually Controlled and Subject to Renewal

Five experiments examined within-event learning in rats by inducing an appetite for one of the elements (salt) of a compound stimulus and assessing preference for the other element (almond). Almond preference was conditional upon (1) the almond flavour having been presented in compound with the salt, and (2) the assessment being conducted when the rats were out of sodium balance (Experiment 1). Presentations of the compound in one environment (A) and of the salt and almond elements in a second environment (B) resulted in greater almond preference when rats were tested in A than in B (Experiment 2). Almond preference was reduced when separate presentations of the compound and almond (Experiment 3) or of the compound and salt (Experiment 4) occurred in the same environments but not when these presentations occurred in different environments. Rats exposed to the compound in A and then extinguished to the elements in either A or B showed a reduced almond preference when tested in the extinction environment, but not when tested in the other environment (Experiment 5). Thus, extinction of within-event learning is context-specific and subject to renewal. The results were interpreted in terms of an associative model whereby separate presentations of the elements result in a symmetrical inhibitory link which is contextually gated (Bouton, 1993).     

Emergence of a cue strategy preference on the water maze task in aged C57B6 x SJL F1 hybrid mice

The effects of age on cue learning, spatial reference memory, and strategy preference were assessed in B6 × SJL F1 mice by using the Morris water maze. This mouse strain is of particular interest because it is the background strain for a common transgenic model of Alzheimer's disease, the Tg2576 mouse, which develops plaques and other neurobiological markers of pathology beginning at 8 mo and increasing in severity with advanced age. In the current study, 12- and 23-mo-old C57B6 × SJL F1 mice were serially trained in cue and place versions of the Morris water maze task. At the completion of training, mice received a strategy probe test in which place (hidden) and cue (visible) strategies were in competition. Cue and spatial learning ability was maintained between 12 and 23 mo of age; however, on the strategy preference probe test, the 23-mo-old mice exhibited a significant bias toward the selection of a cue strategy. There was no relationship between strategy preference in the probe test and spatial learning ability, but the 23-mo-old mice did exhibit a strong trend toward shorter latencies during visible platform training, possibly reflecting the enhanced function of striatal-based neural systems in aging. These data demonstrate that 23-mo-old C57B6 × SJL F1 mice are capable of effective place learning, but if a place strategy is pitted against the use of a cue strategy, the use of a cue strategy predominates in the aged mice. The strategy preference observed here may reflect an emergence of differential processing in underlying brain circuitry with age in the B6 × SJL F1 mouse strain.     

Implicit learning of semantic preferences of English words by Chinese learners

The aim of the present study was to explore whether Chinese learners could implicitly learn the semantic preferences of novel English words. In training, participants learned four novel verbs and were exposed to a set of verb-noun phrases that included these new words. What the participants were not told was that the use of the verbs depended on the concreteness of the nouns (i.e., the semantic preference rule). In testing, participants were required to choose between two possible verbs (one of which violated the semantic preference rule) for nouns that never occurred in training. The results showed that participants acquired unconscious knowledge of semantic preferences under incidental learning conditions, as measured by verbal reports and structural knowledge attributions. Our results provide further evidence for implicit learning of semantic preferences, suggesting that implicit learning is an important mechanism in the acquisition of L2 collocations.     

Memories in drosophila heat-box learning

Learning and memory processes of operant conditioning in the heat-box are analyzed. In a search for conditioning parameters leading to high retention scores, intermittent training is shown to give better results than those of continuous training. Immediate retention tests contain two memory components, a spatial preference for one side of the chamber and a “stay-where-you-are-effect.” Intermittent training strengthens the latter. In the second part, memory dynamics is investigated. Flies are trained in one chamber and tested in a second one after a brief reminder training. With this direct transfer, memory scores reflect an associative learning process in the first chamber. To investigate memory retention after extended time periods, indirect transfer experiments are performed. The fly is transferred to a different environment between training and test phases. With this procedure, an aftereffect of the training can still be observed 2 h later. Surprisingly, exposure to the chamber without conditioning also leads to a memory effect in the indirect transfer experiment. This exposure effect reveals a dispositional change that facilitates operant learning during the reminder training. The various memory effects are independent of the mushroom bodies.     

Complementary roles for the amygdala and hippocampus during different phases of appetitive information processing

Evidence collected from rodent models of memory storage suggests that rapid forms of learning engage the involvement of multiple brain regions each of which may participate in a different component of information processing. The present study used temporary inactivation of the amygdala and hippocampus during different phases of information processing on a one-trial appetitive-conditioning task to examine how these two regions might participate in the storage of appetitive memories. Male Long Evans rats were chronically implanted into the amygdala or dorsal hippocampus and food deprived. Rats were trained on a radial maze conditioned cue preference task where training occurred in one 40-min session and testing took place 24 h later. The amygdala or hippocampus was inactivated separately with muscimol (50 ng/microl) injected immediately before or after training, or immediately before testing. Saline-injected rats displayed a conditioned preference by spending more time in the arm that previously contained food than in the arm that did not contain food. Muscimol injected into the amygdala before training or testing blocked the conditioned preference. Muscimol injected into the hippocampus immediately after training blocked the conditioned preference. These results suggest that the processing of memories may require multiple contributions from separate brain systems for at least short-term (24 h) storage. The resulting output from each system may converge on a similar downstream target to influence behavior.     

Latent spatial learning in an environment with a distinctive shape

Four experiments were conducted with rats in order to determine whether being placed on a platform in one corner of a rectangular swimming pool results in latent spatial learning. Rats in Experiments 1-3 received four trials a day of being placed on the platform. During a subsequent test trial, in which they were released into the pool without the platform, the rats exhibited a preference for swimming in the correct corners of the pool (those with the same geometric properties as the corner containing the platform during training), than the two remaining, incorrect corners. This effect was seen when the interval between the final placement trial and the test trial was as much as 24 hr (Experiment 2) and after varying numbers of sessions of placement training (Experiment 3). Experiment 4 revealed that when the test took place in a kite-shaped arena, after placement training in a rectangle, a stronger preference was shown for the corner that was geometrically equivalent to the correct rather than the incorrect corners in the rectangle. The placement treatment is said to result in latent spatial learning based on the development of S-S associations.     

Socially mediated learning in male Betta splendens. III: Rapid acquisitions

In four experiments with male Siamese fighting fish, the classical conditioning of visual/spatial cues with elicitors of aggression was demonstrated. These studies show that this type of socially mediated learning is more rapidly conditioned than was previously known. One 15-min training session is adequate to condition a preference for those cues that had recently been paired with conspecific images. Finally, behavior occurring during acquisition, in the presence of aggression-eliciting cues, was uncorrelated with the magnitude of the learned preferences that were assayed during extinction tests and in the absence of social stimuli.     

Context conditional flavor preferences in the rat based on fructose and maltodextrin reinforcers

In three experiments, rats were exposed to a flavor preference procedure in which flavor A was paired with the reinforcer and flavor B presented alone in Context 1, while in Context 2 flavor A was presented alone and flavor B with the reinforcer. With fructose as the reinforcer both two- and one-bottle training procedures produced a context-dependent preference (Experiments 1 and 2). With maltodextrin as the reinforcer two-bottle training produced a context-dependent preference (Experiment 1). Following one-bottle training with maltodextrin reinforcement rats demonstrated a context-dependent preference when the conditioned stimulus (CS)- was presented with a dilute solution of the reinforcer during training (Experiment 3B) but not when the CS- was presented alone (Experiments 2 and 3A). The pattern of results with maltodextrin reinforcement suggests that there was competition between the cue flavors and the taste of the maltodextrin as predictors of the postingestive consequences of the maltodextrin reinforcer. The fact that rats were able to display context-dependent flavor preferences is consistent with the idea that learned flavor preferences rely on the sort of cue-consequence associations that underpin other forms of conditioning which produce accurate performance on biconditional tasks. The differences between fructose- and maltodextrin-based preferences are discussed in terms of configural and elemental learning processes.