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Do performance strategies mediate age-related differences in associative learning?

Associative learning is a basic component of most learning tasks and has been shown to decline with age. The authors examined associative learning for younger and older adults by using a noun-pair task. Interim testing and prior practice on a similar task were the manipulated variables. Participants were encouraged to use an efficient retrieval strategy. Interim tests provided the motivation to learn the information, whereas prior practice on a similar task was presumed to make the task easier. The authors examined these variables both independently and interactively. For younger adults, performance benefited little from prior practice but did benefit from interim testing. For older adults, interim tests were beneficial for development of a retrieval strategy irrespective of prior training. Prior training proved beneficial for development of a retrieval strategy in the absence of interim tests. Thus, task parameters influenced the performance strategy (and learning), especially of older adults.

Adolescent↗

Role of the rodent hippocampus in paired-associate learning involving associations between a stimulus and a spatial location.

The ability of rats with control or hippocampal lesions to learn an object-place, odor-place, or object-odor paired-associate task was assessed in a cheeseboard maze apparatus. The data indicate that rats with hippocampal lesions were significantly impaired, compared with controls, in learning both the object-place and the odor-place paired-associate tasks. However, rats with hippocampal lesions learned the object-odor paired-associate task as readily as did controls. The data suggest that the rodent hippocampus is involved in paired-associate learning when a stimulus must be associated with a spatial location. However, the hippocampus is not involved in paired-associate learning when the association does not involve a spatial component.

Animals↗

Effects of associative learning on age differences in task-set switching.

Costs of switching between tasks may disappear when subjects are able to learn associations between tasks, stimuli, and responses (cf. Rogers, R. D., & Monsell, S. (1995). Costs of a predictable switch between simple cognitive tasks. Journal of Experimental Psychology: General, 124, 207-231). The first aim of this study was to examine this possibility by manipulating stimulus-set size. We expected that costs of switching between tasks would be strongly reduced under conditions of small stimulus-set sizes (n=4) as compared to large stimulus-set sizes (n=96) with increasing time on task. The second aim was to determine whether younger as well as older adults were able to create associations between task components. As age differences in task switching are often found to be larger when response mappings are incompatible we also investigated interactions with response compatibility. Results of our study indicated that practice effects on switch costs were much more pronounced for small than large stimulus-set sizes, consistent with the view that the strength of associations between task components facilitates task switching. Furthermore, we found that practice benefits on task switching for small stimulus-set sizes were sensitive to age and response compatibility. In contrast to younger adults, who showed a reduction of switch costs for both response mapping conditions, older adults showed a reduction of switch costs only when response mappings were compatible. That is, older adults showed less associative learning when the currently irrelevant task feature had to be suppressed, supporting the view that older adults have primarily problems in separating overlapping task-set representations.

Adult↗

Visual-visual associative learning and reward-association learning in monkeys: the role of the amygdala.

Three Cynomolgus monkeys (Macaca fascicularis) took part in an experiment on visual learning set in an automatic apparatus. Each new visual discrimination problem was solved using a visual secondary reinforcer consisting of a white line. If the monkey chose the correct stimulus (by touching it), the white line appeared over the correct stimulus. Primary food reward was delivered only after a new problem was solved to a criterion, and the problem was then replaced by a new one. Thus, within-problem learning did not rely on primary reinforcement but on the visual secondary reinforcer. The animals were trained preoperatively in visual learning set with this procedure and were assessed postoperatively for their ability to learn new visual discriminations with the same procedure. Bilateral amygdalectomy did not significantly impair the animals' learning ability in this task. Learning remained unimpaired when transection of the uncinate fascicle and of the fornix was added to amygdalectomy. The effect of bilateral amygdalectomy in this task was much less severe than in a similar task we previously studied, with auditory secondary reinforcers. The results show that the involvement of the amygdala in processes of secondary reinforcement depends on the sensory properties of the secondary reinforcer. From these and other recent results, we conclude that the sensory attributes of a reinforcer are easily associated with a discriminative stimulus when they are in the same modality and same spatial location as the discriminative stimulus and that this sensory-sensory association is independent of the amygdala.

Amygdala↗

Is tube-escape learning by protozoa associative learning?

The ciliate protozoa, Stentor and Paramecium, have been reported to escape from the bottom end of narrow capillary tubes into a larger volume of medium with increasing rapidity over the course of trials. This change in behavior has been considered an apparent example of associative learning. This decrease in escape time is not due to a change in the protozoa's environment, their swimming speed, frequency of ciliary reversals, or the proportion of time spent forward or backward swimming. Instead, most of the decrease results from a decrease in the proportion of time spent in upward swimming. However, a similar decrease in upward swimming occurs when the task is altered to require escape from the upper end of the capillary tubes. Because the protozoa exhibit the same change in behavior regardless of the reinforcing stimulus, tube-escape learning is not associative learning.

Animals↗

Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus-action-reward association learning.

To select appropriate behaviors leading to rewards, the brain needs to learn associations among sensory stimuli, selected behaviors, and rewards. Recent imaging and neural-recording studies have revealed that the dorsal striatum plays an important role in learning such stimulus-action-reward associations. However, the putamen and caudate nucleus are embedded in distinct cortico-striatal loop circuits, predominantly connected to motor-related cerebral cortical areas and frontal association areas, respectively. This difference in their cortical connections suggests that the putamen and caudate nucleus are engaged in different functional aspects of stimulus-action-reward association learning. To determine whether this is the case, we conducted an event-related and computational model-based functional MRI (fMRI) study with a stochastic decision-making task in which a stimulus-action-reward association must be learned. A simple reinforcement learning model not only reproduced the subject's action selections reasonably well but also allowed us to quantitatively estimate each subject's temporal profiles of stimulus-action-reward association and reward-prediction error during learning trials. These two internal representations were used in the fMRI correlation analysis. The results revealed that neural correlates of the stimulus-action-reward association reside in the putamen, whereas a correlation with reward-prediction error was found largely in the caudate nucleus and ventral striatum. These nonuniform spatiotemporal distributions of neural correlates within the dorsal striatum were maintained consistently at various levels of task difficulty, suggesting a functional difference in the dorsal striatum between the putamen and caudate nucleus during stimulus-action-reward association learning.

Adult↗

Selective remodeling of rabbit frontal cortex: relationship between 5-HT2A receptor density and associative learning.

RATIONALE: Associative learning during classical trace eyeblink conditioning has been shown to be regulated by serotonin 5-HT(2A )receptors and to be critically dependent on the integrity of frontal cortex. Chronic administration of 5-HT(2A) ligands has been shown to produce a selective up- or down-regulation of 5-HT(2A) receptors in frontal cortex. OBJECTIVES: We examined whether alterations in 5-HT(2A) receptor density had a functional significance with respect to associative learning. METHODS: Animals received chronic injections of LSD, BOL or MDL11,939 and 1 day later began classical trace conditioning of the eyeblink response. RESULTS: The density of 5-HT(2A) receptors in frontal cortex was significantly increased at 1-4 days after the cessation of chronic injections of the selective 5-HT(2A) receptor ligand MDL11,939. Rabbits demonstrated an enhancement of associative learning when training began at 1 day after cessation of chronic MDL11,939 injections, but acquired at the same rate as controls when training began at 8 days after cessation of injections, a time when receptor density had returned to control levels. Animals that began training 1 day after chronic injections of BOL or LSD, drugs that produce decreases in 5-HT(2A) receptor density, demonstrated normal rates of acquisition. CONCLUSIONS: These results indicate that increases in the density of 5-HT(2A) receptors in frontal cortex are associated with increases in the rate of associative learning, and further support an important role for this receptor in cortical circuitry that mediates learning. More generally, these results suggest an approach for functional remodeling of brain regions in the adult animal.

Animals↗

The neuroscience of mammalian associative learning.

Mammalian associative learning is organized into separate anatomically defined functional systems. We illustrate the organization of two of these systems, Pavlovian fear conditioning and Pavlovian eyeblink conditioning, by describing studies using mutant mice, brain stimulation and recording, brain lesions and direct pharmacological manipulations of specific brain regions. The amygdala serves as the neuroanatomical hub of the former, whereas the cerebellum is the hub of the latter. Pathways that carry information about signals for biologically important events arrive at these hubs by circuitry that depends on stimulus modality and complexity. Within the amygdala and cerebellum, neural plasticity occurs because of convergence of these stimuli and the biologically important information they predict. This neural plasticity is the physical basis of associative memory formation, and although the intracellular mechanisms of plasticity within these structures share some similarities, they differ significantly. The last Annual Review of Psychology article to specifically tackle the question of mammalian associative learning ( Lavond et al. 1993 ) persuasively argued that identifiable "essential" circuits encode memories formed during associative learning. The next dozen years saw breathtaking progress not only in detailing those essential circuits but also in identifying the essential processes occurring at the synapses (e.g., Bi & Poo 2001, Martinez & Derrick 1996 ) and within the neurons (e.g., Malinow & Malenka 2002, Murthy & De Camilli 2003 ) that make up those circuits. In this chapter, we describe the orientation that the neuroscience of learning has taken and review some of the progress made within that orientation.

Animals↗

Post-session sulpiride infusions within the perifornical region of the lateral hypothalamus enhance consolidation of associative learning.

Whilst neurons within the lateral hypothalamus are well known to be responsive to the presentation of previously learned associative stimuli, the consolidation of a Pavlovian association is thought to depend in large part upon other brain regions, including the amygdala. The present study addressed this assumption directly, by examining the effect of post-session infusions of sulpiride within the lateral hypothalamus upon the acquisition of a conditioned approach response in an appetitive differential conditioning task. Subjects were exposed to an initially neutral stimulus (CS+), which immediately preceded the availability of a 10% sucrose reward (US). A second, control stimulus (CS ) was also presented. but never in close temporal proximity to the US. The number and duration of alcove approaches were recorded. Immediately following each training session, subjects were infused bilaterally with sulpiride (0, 0.5, 5 microg) in the vicinity of the perifornical region of the lateral hypothalamus. Sulpiride dose-dependently enhanced the rate of acquisition of a conditioned approach response to presentation of the CS+, but was without affect upon approach behaviour during CS(-) or US presentations. Thus, 0.5 microg sulpiride facilitated at an early stage (session 2 onwards) the number of alcove approaches to the CS+, while 5 microg sulpiride enhanced to a greater extent the duration of conditioned approach, particularly during later sessions. A subsequent locomotor test using 0.5 mg/kg d-amphetamine indicated that repeated infusions of the higher dose sulpiride (5 microg), but not the lower dose (0.5 microg), resulted in behavioural sensitisation to administration of the psychomotor stimulant. Acquisition of a novel conditioned instrumental response was not affected by previous exposure to sulpiride. These data suggest that dopamine-sensitive neurons within the lateral hypothalamus may play a significant role in the acquisition of appetitive Pavlovian associations.

Animals↗

Implicit associative learning engages the hippocampus and interacts with explicit associative learning.

The hippocampus is crucial for conscious, explicit memory, but whether it is also involved in nonconscious, implicit memory is uncertain. We investigated with functional magnetic resonance imaging whether implicit learning engages the hippocampus and interacts with subsequent explicit learning. The presentation of subliminal faces-written profession pairs for implicit learning was followed by the explicit learning of supraliminal pairs composed of the same faces combined with written professions semantically incongruous to those presented subliminally (experiment 1), semantically congruous professions (experiment 2), or identical professions (experiment 3). We found that implicit face-profession learning interacted with explicit face-profession learning in all experiments, impairing the explicit retrieval of the associations. Hippocampal activity increased during the subliminal presentation of face-profession pairs versus face-nonword pairs and correlated with the later impairment of explicit retrieval. These findings suggest that implicit semantic associative learning engages the hippocampus and influences explicit memory.

Association Learning↗

Perirhinal cortex ablation impairs configural learning and paired-associate learning equally.

Combined damage to the perirhinal and entorhinal cortex has been implicated in the formation of stimulus-stimulus associative memories. We show in this article that relative to three normal controls three cynomolgus monkeys with ablations restricted to the perirhinal cortex were impaired on a visual paired associate learning task in which subjects had to learn which of two visual stimuli were associated with a cue stimulus. The subjects with perirhinal cortex ablations also showed an impairment of a similar magnitude on a visual configural learning task in which they had to learn which of two configurations of visual stimuli were associated with food-reward. The stimuli in both tasks were comprised of alphanumeric characters presented upon a touch-screen. Both groups made fewer errors on the configural learning task than on the paired associate learning task. We suggest that performance on both tasks relies critically on the perirhinal cortex due to the specialization of the perirhinal cortex in processing knowledge about objects. We argue that the specializations of this system and of other memory systems such as the hippocampal-fornix spatial/episodic memory system, are conferred by the specialization of their anatomical connections to other structures. We reject the notion that there are specific memory processes such as the hippocampal based configural associative system that was proposed to be critical for configural associative learning.

Animals↗

Secondary structure and Ca2+-induced conformational change of calexcitin, a learning-associated protein.

Calexcitin/cp20 is a low molecular weight GTP- and Ca2+-binding protein, which is phosphorylated by protein kinase C during associative learning, and reproduces many of the cellular effects of learning, such as the reduction of potassium currents in neurons. Here, the secondary structure of cloned squid calexcitin was determined by circular dichroism in aqueous solution and by Fourier transform infrared spectroscopy both in solution and on dried films. The results obtained with the two techniques are in agreement with each other and coincide with the secondary structure computed from the amino acid sequence. In solution, calexcitin is one-third in alpha-helix and one-fifth in beta-sheet. The conformation of the protein in solid state depends on the concentration of the starting solution, suggesting the occurrence of surface aggregation. The secondary structure also depends on the binding of calcium, which causes an increase in alpha-helix and a decrease in beta-sheet, as estimated by circular dichroism. The conformation of calexcitin is independent of ionic strength, and the calcium-induced structural transition is slightly inhibited by Mg2+ and low pH, while favored by high pH. The switch of calexcitin's secondary structure upon calcium binding, which was confirmed by intrinsic fluorescence spectroscopy and nondenaturing gel electrophoresis, is reversible and occurs in a physiologically meaningful range of Ca2+ concentration. The calcium-bound form is more globular than the apoprotein. Unlike other EF-hand proteins, calexcitin's overall lipophilicity is not affected by calcium binding, as assessed by hydrophobic liquid chromatography. Preliminary results from patch-clamp experiments indicated that calcium is necessary for calexcitin to inhibit potassium channels and thus to increase membrane excitability. Therefore the calcium-dependent conformational equilibrium of calexcitin could serve as a molecular switch for the short term modulation of neuronal activity following associative conditioning.

Amino Acid Sequence↗

Learned associability and associative change in human causal learning.

The Mackintosh (1975) model of associative learning specifies that processing of both the cues presented on a trial and the outcome of that trial will interact to determine the amount of associative change undergone by a given cue. Experiments looking at the distribution of associative change among the elements of a reinforced compound in animal conditioning studies indicate that processing of the outcome of a trial does indeed influence associative change. The work reported here investigates the distribution of associative change among the elements of a reinforced compound in a human causal judgement paradigm, and it indicates that processing of the cues presented on a trial also plays a role in determining associative change (in terms of changes in the associability of cues as a result of experience). Taken in combination, these results provide good support for Mackintosh (1975) and the characterizations of both cue and outcome processing that it offers.

Adult↗

Neurons in human temporal cortex active with verbal associative learning.

In neuronal activity recorded from human middle temporal gyrus during learning of associations between word pairs, a population was identified that had greater activity for associations that were learned rapidly during initial encoding compared to those learned slowly or not at all by an individual subject. This population can be separated from other neurons by the combination of inhibition during word reading when no learning is required and excitation during recent memory for words. These neurons are present in both hemispheres, predominately in deeper layers of cortex. During initial encoding, the increased activity appears at presentation of all word pairs but persists for several seconds only for the rapidly learned pairs, likely reflecting rehersal of items being learned. Human associative learning is related to activity of this specific population of "association" neurons, identified here for the first time.

Adult↗

Effects of contextual processing on visual conditional associative learning in schizophrenia.

BACKGROUND: We adapted visual conditional associative learning paradigms to assess the contextual processing deficit model of schizophrenic cognitive impairment proposed by J.D. Cohen and D. Servan-Schreiber in 1992. In this task subjects learn the associations between four sets of stimuli through the use of feedback. We administered two experimental conditional associative learning conditions: in one, the eight stimuli used to make four pairs were all different; in the other, the pairs were made from different combinations of four identical stimuli, requiring the use of contextual information to mediate correct performance. Two additional associative learning tasks were administered where subjects generated the stimulus pairings or observed the experimenter form the pairs, eliminating the need to learn from feedback. METHODS: We tested 37 patients with schizophrenia and 20 healthy control subjects in each conditional associative learning task condition. RESULTS: Patients demonstrated significant impairments on all four conditional associative learning tasks. The demand to process contextual information did not differentially impact patient performance. Patients were better able to learn associations if they generated or observed the pairings rather than utilized feedback to guide learning. CONCLUSIONS: Patients with schizophrenia demonstrate pronounced deficits in the ability to utilize feedback to guide learning. We found no evidence of an additional deficit in processing of contextual information.

Adult↗

Associative learning: Hebbian flies.

Fruit flies can learn to associate an odor with an aversive stimulus, such as a shock. New findings indicate that disrupting the expression of N-methyl-D-aspartate (NMDA) receptors in flies impairs olfactory conditioning. The findings provide support for a critical role for NMDA receptors in associative learning.

Animals↗

Critical role of the parahippocampal region for paired-associate learning in rats.

Human amnesics are severely impaired in learning arbitrary associations between word pairs. This report examines the role of the hippocampal system in an analog of paired-associate learning developed for rats. Subjects with selective damage to the parahippocampal region and controls were tested on an odor-guided paired-associate task. Normal rats readily learned to distinguish paired associates from various mispairings of the same odors, whereas most animals with parahippocampal damage failed to learn. Lesioned animals were, however, able to acquire correct responses to stimulus pairs for which an association between odors was not required. These findings extend the usefulness of olfactory learning as a model for studies of higher order learning capacity in rodents and indicate that in rats, as in humans, hippocampal areas are critical for learning arbitrary nonspatial relationships between stimuli.

Animals↗