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Fear conditioning induces a lasting potentiation of synaptic currents in vitro.

The amygdala plays a critical role in the mediation of emotional responses, particularly fear, in both humans and animals. Fear conditioning, a conditioned learning paradigm, has served as a model for emotional learning in animals, and the neuroanatomical circuitry underlying the auditory fear-conditioning paradigm is well characterized. Synaptic transmission in the medial geniculate nucleus (MGN) to lateral nucleus of the amygdala (LA) pathway, a key segment of the auditory fear conditioning circuit, is mediated largely through N-methyl-D-aspartate (NMDA) and non-NMDA (such as alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)) glutamate receptors; the potential for neural plasticity in this pathway is suggested by its capacity to support long-term potentiation (LTP). Here we report a long-lasting increase in the synaptic efficacy of the MGN-LA pathway attributable to fear-conditioning itself, rather than an electrically induced model of learning. Fear-conditioned animals show a presynaptic facilitation of AMPA-receptor-mediated transmission, directly measured in vitro with whole-cell recordings in lateral amygdala neurons. These findings represent one of the first in vitro measures of synaptic plasticity resulting from emotional learning by whole animals.

Amygdala↗

On the role of the hippocampus in learning and memory in the rat.

An overview of lesion experiments concerned with the involvement of the hippocampus in learning and memory in the rat is presented. Multiple injections of small amounts of ibotenic acid were used to selectively remove the hippocampus (dentate gyrus, hilar cells, CA1-CA3 pyramidal cells). Similar selective, axon-sparing ibotenate lesions of hippocampus were used in a series of learning and memory experiments employing tasks that are thought to be important in hippocampal function. The performance of rats with the hippocampus removed was compared with that of control animals in the acquisition and retention of spatial versus nonspatial information, forgetting of spatial and nonspatial information, contextual learning, recognition memory and concurrent discrimination learning, and complex representational learning (conditional discrimination and negative patterning learning). The general finding that rats without a hippocampus were impaired on those tasks that required the utilization of spatial and contextual information stands in contrast with the spared performance that was found in learning about and handling (even complex) nonspatial information. Rather than support for views that emphasize a role for the hippocampus in specific memory processes (working memory, declarative memory, temporary memory buffer, configural learning), the present results are more compatible with the idea that the hippocampus plays an especially important role in processing and remembering spatial and contextual information. The limited data that are available using more selective lesions of related hippocampal formation structures (entorhinal cortex, subiculum) suggest that these structures also make important contributions to learning and memory, and that some of these contributions may be different from those made by the hippocampus.

Animals↗

Learning versus correct models: influence of model type on the learning of a free-weight squat lift.

It has been assumed that demonstrating the correct movement is the best way to impart task-relevant information. However, empirical verification with simple laboratory skills has shown that using a learning model (showing an individual in the process of acquiring the skill to be learned) may accelerate skill acquisition and increase retention more than using a correct model. The purpose of the present study was to compare the effectiveness of viewing correct versus learning models on the acquisition of a sport skill (free-weight squat lift). Forty female participants were assigned to four learning conditions: physical practice receiving feedback, learning model with model feedback, correct model with model feedback, and learning model without model feedback. Results indicated that viewing either a correct or learning model was equally effective in learning correct form in the squat lift.

Analysis of Variance↗

Individual differences in working memory capacity and learning: evidence from the serial reaction time task.

High and low working memory (WM) capacity individuals performed the serial reaction time task under both incidental and intentional learning conditions to determine the role of WM capacity in the learning of sequential information. WM capacity differences emerged in conditions of intentional but not incidental learning, indicating that individual differences in WM capacity occur in tasks requiring some form of control, with little difference appearing on tasks that required relatively automatic processing. Furthermore, an index of learning was significantly related to a measure of general fluid intelligence under intentional conditions only. Thus, the degree of learning was significantly related to higher order cognition, but only when intentional processing was emphasized.

Awareness↗

Processing demands during auditory learning under degraded listening conditions.

This investigation employed measures of learning accuracy (performance) and learning ease (attention or psychological effort) to assess processing demands during auditory learning under degraded listening conditions. Learning accuracy was measured with a highly intelligible paired-associate learning task presented to 49 normal-hearing adults under different signal-to-competition ratios and signal presentation levels. Learning ease was assessed by a simultaneously presented probe reaction-time task. Final results indicated that (1) primary signal presentation level exerted no effect either on learning accuracy or ease, and (2) the introduction of competing speech into the listening environment exerted no effect on learning performance, but resulted in a significant increase in learning effort. These findings have important implications for listening conditions in educational settings, hearing aid selection, education of hearing-impaired and learning-disabled children, and future study of attentional demands during auditory processing.

Adult↗

Repeated acquisition of response sequences: stimulus control and drugs.

Pigeons obtained food by making four responses on three keys in a specified sequence, e.g., left, right, center, right. Under the "tandem-learning" condition, all three keys were the same color throughout the response sequence, and the sequence was changed from session to session. After total errors per session (overall accuracy) and within-session error reduction (learning) had stabilized, the effects of varying doses phenobarbital and chlordiazepoxide were assessed. For comparison, the drug tests were also conducted under a "tandem-performance" condition, in which the response sequence was the same from session to session, and under corresponding "chain-learning" and "chain-performance" conditions, where different colored keylights were associated with the response sequence. Under all four baseline conditions, the largest dose of each drug impaired overall accuracy. Under the two learning conditions, the error rate decreased across trials within each session, but the degree of negative acceleration was less in the drug sessions than in the control sessions. In contrast, under the two performance conditions, the error rate was relatively constant across trials, but was higher in the drug sessions than in the control sessions. Of the four baselines, the chain-learning condition was the most sensitive to the drug effects.

Animals↗

How the basal ganglia use parallel excitatory and inhibitory learning pathways to selectively respond to unexpected rewarding cues.

After classically conditioned learning, dopaminergic cells in the substantia nigra pars compacta (SNc) respond immediately to unexpected conditioned stimuli (CS) but omit formerly seen responses to expected unconditioned stimuli, notably rewards. These cells play an important role in reinforcement learning. A neural model explains the key neurophysiological properties of these cells before, during, and after conditioning, as well as related anatomical and neurophysiological data about the pedunculopontine tegmental nucleus (PPTN), lateral hypothalamus, ventral striatum, and striosomes. The model proposes how two parallel learning pathways from limbic cortex to the SNc, one devoted to excitatory conditioning (through the ventral striatum, ventral pallidum, and PPTN) and the other to adaptively timed inhibitory conditioning (through the striosomes), control SNc responses. The excitatory pathway generates CS-induced excitatory SNc dopamine bursts. The inhibitory pathway prevents dopamine bursts in response to predictable reward-related signals. When expected rewards are not received, striosomal inhibition of SNc that is unopposed by excitation results in a phasic drop in dopamine cell activity. The adaptively timed inhibitory learning uses an intracellular spectrum of timed responses that is proposed to be similar to adaptively timed cellular mechanisms in the hippocampus and cerebellum. These mechanisms are proposed to include metabotropic glutamate receptor-mediated Ca(2+) spikes that occur with different delays in striosomal cells. A dopaminergic burst in concert with a Ca(2+) spike is proposed to potentiate inhibitory learning. The model provides a biologically predictive alternative to temporal difference conditioning models and explains substantially more data than alternative models.

Animals↗

Reversal of long-delay conditioned taste aversion learning in rats by sex hormone manipulation.

Conditioned taste aversion (CTA) learning is an adaptive, robust, well-established learning and memory paradigm. Strong taste aversions develop to the conditioned stimulus (CS = saccharin) despite long delays between exposure to the CS and unconditioned stimulus (US = LiCl). Rats display a sexually dimorphic pattern of long-delay CTA learning (Foy et al., 1996). The present study examines whether this sex difference is a result of activational or organizational hormone action, because here we implanted gonadectomized rats with their normal hormone replacements, or with opposing hormones prior to testing in a 4-hr delayed CTA learning task. We found that gonadally intact male rats displayed a more robust CTA response than intact female rats. Gonadectomy essentially eliminated this sex difference; gonadectomized males and gonadectomized females displayed similar CTA responses. In gonadectomized rats, when their normal sex hormones were replaced with implanted hormone pellets, the sex difference in CTA learning was reinstated. In contrast, when gonadectomized rats were implanted with opposing hormones, the sex difference was reversed. Gonadectomized female rats implanted with 5alpha-DHT pellets (metabolite of testosterone) displayed a stronger CTA response compared to gonadectomized males implanted with 17beta-estradiol pellets. Regardless of the original developmental hormonal environment, our study suggests that an activational manipulation of circulating hormones serves to significantly influence long-delay CTA learning in rats.

Androgens↗

Taste-aversion conditioning with expected versus unexpected drug treatment.

Following differential conditioning in which a drug-predictive taste solution (D) infused into the oral cavity of rats was followed by a lithium injection and a no-drug-predictive solution (ND) was not reinforced, animals received a backward pairing between lithium and a novel saccharin flavor. Subjects infused with either the D solution or tap water immediately before backward conditioning learned weaker saccharin aversions than animals infused with the ND solution and animals given no infusion at this time (Experiments 1 and 3). These latter groups did not differ from each other (Experiment 3). The interference with aversion learning produced by water infusion appeared to be due to conditioned excitation that accrued to sensations of the infusion process. Extinction of the infusion sensations eliminated blocking produced by the infusion of water (Experiments 4 and 5). The blocking of saccharin-aversion learning produced by infusion of the D solution was due, to a large extent, to the conditioned aversiveness of the D taste. Extinction of the aversion to the D taste eliminated the interference with saccharin conditioning (Experiment 2), whereas extinction of the excitatory properties of the infusion process did not prevent the blocking of conditioning by infusion of the D solution (Experiment 5). These results are inconsistent with suggestions that taste-aversion learning is a primitive form of conditioning; rather, they demonstrate the influence of informational variables on conditioned taste aversions.

Administration, Oral↗

Pavlovian conditioning: a functional perspective.

From a functional perspective, Pavlovian conditioning involves learning about conditioned stimuli (CSs) that have a pre-existing relation to an unconditioned stimulus (US) rather than learning about arbitrary or neutral CSs. In addition, the most important product of learning involves changes in how the organism responds to the US, not in how it responds to the CS, because the US is the more biologically relevant stimulus. These concepts are illustrated using examples from a variety of behavioral and physiological situations including caloric intake and digestion, breast feeding, poison-avoidance learning, eyeblink conditioning, sexual conditioning, fear conditioning, aggression, and drug tolerance and sensitization.

Adaptation, Psychological↗

Adventitious control by the location of comparison stimuli in conditional discriminations.

In a conditional discrimination procedure, samples appeared in a center key, and comparisons appeared in two of four outer keys. The location of comparison keys varied from trial to trial. Separate learning curves for each of the six possible pairs of comparison keys were plotted in a signal-detection space, revealing different patterns of progress on each pair. Also, when learned conditional discriminations were disrupted, pairs of keys differed in their patterns of disruption. Varying the location of comparison stimuli among six different pairs of keys had not eliminated key position as a controlling aspect of the stimuli. The variations simply increased the number of stimulus compounds--key position and experimental stimuli--that the subject learned. Plotting conditional-discrimination learning curves in a signal-detection space reveals relations among hits, false alarms, accuracy, and comparison preference that help to define a subject's progress.

Animals↗

Rat amygdaloid neuron responses during auditory discrimination.

To investigate amygdaloid contribution to stimulus-affect association and to emotional behavior, single neuron activity was recorded in the basolateral and corticomedial amygdala of the rat amygdala during discrimination of conditioned cue tones associated with positive (glucose and intracranial self-stimulation) and negative (weak electric footshock) unconditioned stimuli. Amygdaloid neurons that responded to two rewarding unconditioned stimuli responded in the same manner to both. Responses to conditioned cue tones and those to rewards were also significantly related, suggesting that amygdaloid neuronal responses to conditioned stimuli are closely related to the affective nature of the corresponding unconditioned stimulation. These might be neuronal functions that underlie stimulus-affect association in the amygdala. In random repeated trials, including acquisition to conditioned cue tones and extinction after acquisition, response plasticity was more evident in basolateral than in corticomedial neurons. Furthermore, more basolateral than corticomedial neurons differentiated glucose and its cue from intracranial self-stimulation and its cue by responding to one but not the other. More basolateral than corticomedial neurons were excited by intracranial self-stimulation and its cue and inhibited by footshock and its cue. The differences between the two nuclear groups suggest that basolateral neurons are more plastic and discriminative, and corticomedial neurons respond indiscriminately to positive and negative unconditioned or conditioned stimuli. The results indicate amygdaloid neuron involvement in stimulus-affect association. Basolateral neurons may be more involved than corticomedial neurons in discriminating and learning conditioned stimuli.

Acoustic Stimulation↗

Associative memory in three aplysiids: correlation with heterosynaptic modulation.

Much recent research on mechanisms of learning and memory focuses on the role of heterosynaptic neuromodulatory signaling. Such neuromodulation appears to stabilize Hebbian synaptic changes underlying associative learning, thereby extending memory. Previous comparisons of three related sea-hares (Mollusca, Opisthobranchia) uncovered interspecific variation in neuromodulatory signaling: strong in Aplysia californica, immeasureable in Dolabrifera dolabrifera, and intermediate in Phyllaplysia taylori. The present study addressed whether this interspecific variation in neuromodulation is correlated with memory of associative (classical conditioning) learning. We differentially conditioned the tail-mantle withdrawal reflex of each of the three species: Mild touch to one side of the tail was paired with a noxious electrical stimulus to the neck. Mild touch to the other side served as an internal control. Post-training reflex amplitudes were tested 15-30 min after training and compared with pre-test amplitudes. All three species showed conditioning: training increased the paired reflex more than the unpaired reflex. However, the temporal pattern of conditioning varied between species. Aplysia showed modest conditioning that grew across the post-test period. Dolabrifera showed distinctly short-lived conditioning, present only on the first post-test. The time course of memory in Phyllaplysia was intermediate, although not statistically distinguishable from the other two species. Taken together, these experiments suggest that evolutionary changes in nonassociative heterosynaptic modulation may contribute to evolutionary changes in the stability of the memory of classical conditioning.

Animals↗

Pattern learning by honeybees: conditioning procedure and recognition strategy.

In recognizing a pattern, honeybees Apis mellifera, may focus either on its ventral frontal part, or on the whole frontal image. We asked whether the conditioning procedure used to train the bees to a pattern determines the recognition strategy employed. Bees were trained with the same patterns presented vertically on the back walls of a Y maze. Conditioning was either absolute, that is, bees should learn to choose a rewarded pattern when there is no alternative, or differential, that is, bees should learn to choose a rewarded pattern that is paired with a different, nonrewarded one. Bees used different pattern recognition strategies depending on the conditioning procedure: absolute conditioning restricted recognition to the lower half whilst differential conditioning extended it to the whole pattern. Bees trained with absolute conditioning saw and learned the features of the upper part of the trained patterns, but assigned more weight to the lower part. Bees trained with differential conditioning learned not only the features of the reinforced stimulus in an excitatory way, but also those of the nonreinforced one in an inhibitory way. Thus, conditioning tasks that involve not only excitatory acquisition of the conditioned stimulus per se, but also discrimination of nonreinforced stimuli, result in an increase in the visual field assigned to the recognition task. Conditioning tasks that involve only excitatory acquisition of the rewarded stimulus result in a higher weighting of the lower pattern half and thus in a more reduced field assigned to the recognition task. This difference may reflect that existing between a conditioned and an incidental behavioural modification. Copyright 1999 The Association for the Study of Animal Behaviour.

Journal Article↗

[The effect of phenamine and caffeine on caudate inhibition of conditioned reflex avoidance reactions in cats].

In cats with a preliminarily learned conditioned avoidance reaction, stimulation of the caudate nucleus inhibited behavioral response by lengthening its latency and reducing the number of conditioned reactions. Intensity of the inhibitory effect did not substantially depend on the localization of electrodes in the head or body of the nucleus and weakened within a few experimental days. D,1-amphetamine (0.5 to 4 mg/kg) and caffeine (10 to 10 mg/kg) suppressed the caudate inhibition, but the action of the drugs was manifested in different ways. The influence of large doses of d,1-amphetamine was characterized by a serious disturbance of behaviour and caudate inhibition of conditioned responses.

Amphetamine↗

Genetic dissection of consolidated memory in Drosophila.

Behavioral and pharmacological experiments in many animal species have suggested that memory is consolidated from an initial, disruptable form into a long-lasting, stable form within a few hours after training. We combined these traditional approaches with genetic analyses in Drosophila to show that consolidated memory of conditioned (learned) odor avoidance 1 day after extended training consisted of two genetically distinct, functionally independent memory components: anesthesia-resistant memory (ARM) and long-term memory (LTM). ARM decayed away within 4 days, was resistant to hypothermic disruption, was insensitive to the protein synthesis inhibitor cycloheximide (CXM), and was disrupted by the radish single-gene mutation. LTM showed no appreciable decay over 7 days, was sensitive to CXM, and was not disrupted by the radish mutation.

Animals↗