Reward enhancement of item-location associative memory spreads to similar items within a category.

The experience of a reward appears to enhance memory for recent prior events, adaptively making that information more available to guide future decision-making. Here, we tested whether reward enhances memory for associative item-location information and also whether the effect of reward spreads to other categorically-related but unrewarded items. Participants earned either points (Experiment 1) or money (Experiment 2) through a time-estimation reward task, during which stimuli-location pairings around a 2D-ring were shown followed by either high-value or low-value rewards. All stimuli were then tested for location memory or recognition (yes/no), immediately and after a 24-hour delay. Across both experiments (combined analysis), there was a robust improvement in location memory following high-value rewards, even though evidence supporting this effect was reliable in Experiment 2 but not in Experiment 1. The memory-enhancing effect of reward was observed on both the immediate and delayed location-memory tests. Reward-enhanced memory for both directly rewarded stimuli and categorically related stimuli that were not directly rewarded. No reliable effect of reward value on yes/no recognition-memory performance was observed in either experiment. We hypothesise that reward enhances the consolidation of recent experience and conceptually related memories to make these more available for future decisions.

Motor precision deficits in clinical high risk for psychosis.

Motor deficits appear prior to psychosis onset, provide insight into vulnerability as well as mechanisms that give rise to emerging illness, and are predictive of conversion. However, to date, the extant literature has often targeted a complex abnormality (e.g., gesture dysfunction, dyskinesia), or a single fundamental domain (e.g., accuracy) but rarely provided critical information about several of the individual components that make up more complex behaviors (or deficits). This preliminary study applies a novel implicit motor task to assess domains of motor accuracy, speed, recognition, and precision in individuals at clinical high risk for psychosis (CHR-p). Sixty participants (29 CHR-p; 31 healthy volunteers) completed clinical symptom interviews and a novel Serial Interception Sequence Learning (SISL) task that assessed implicit motor sequence accuracy, speed, precision, and explicit sequence recognition. These metrics were examined in multilevel models that enabled the examination of overall effects and changes in motor domains over blocks of trials and by positive/negative symptom severity. Implicit motor sequence accuracy, speed, and explicit sequence recognition were not detected as impacted in CHR-p. When compared to healthy controls, individuals at CHR-p were less precise in motor responses both overall (d = 0.91) and particularly in early blocks which normalized over later blocks. Within the CHR-p group, these effects were related to positive symptom levels (t = - 2.22, p = 0.036), such that individuals with higher symptom levels did not improve in motor precision over time (r's = 0.01-0.05, p's > 0.54). CHR-p individuals showed preliminary evidence of motor precision deficits but no other motor domain deficits, particularly in early performance that normalized with practice.

Separate Memory-Enhancing Effects of Reward and Strategic Encoding.

Memory encoding for important information can be enhanced both by reward anticipation and by intentional strategies. These effects are hypothesized to depend on distinct neural mechanisms, yet prior work has provided only limited evidence for their separability. We aimed to determine whether reward-driven and strategic mechanisms for prioritizing important information are separable, even if they may also interact. We examined the joint operation of both mechanisms using fMRI measures of brain activity. Participants learned abstract visual images in a value-directed recognition paradigm. On each trial, two novel images were presented simultaneously in different screen quadrants, one arbitrarily designated as high point value and one as low value. Immediately after each block of 16 study trials, the corresponding point rewards could be obtained in a test of item recognition and spatial location memory. During encoding trials leading to successful subsequent memory, especially of high-value images, increased activity was observed in dorsal frontoparietal and lateral occipitotemporal cortex. Furthermore, activity in a network associated with reward was higher during encoding when any image, of high or low value, was subsequently remembered. Functional connectivity between right medial temporal lobe and right ventral tegmental area, measured via psychophysiological interaction, was also greater during successful encoding regardless of value. Strategic control of memory, as indexed by successful prioritization of the high-value image, affected activity in dorsal posterior parietal cortex as well as connectivity between this area and right lateral temporal cortex. These results demonstrate that memory can be strengthened by separate neurocognitive mechanisms for strategic control versus reward-based enhancement of processing.

Functional differences between statistical learning with and without explicit training.

Humans are capable of rapidly extracting regularities from environmental input, a process known as statistical learning. This type of learning typically occurs automatically, through passive exposure to environmental input. The presumed function of statistical learning is to optimize processing, allowing the brain to more accurately predict and prepare for incoming input. In this study, we ask whether the function of statistical learning may be enhanced through supplementary explicit training, in which underlying regularities are explicitly taught rather than simply abstracted through exposure. Learners were randomly assigned either to an explicit group or an implicit group. All learners were exposed to a continuous stream of repeating nonsense words. Prior to this implicit training, learners in the explicit group received supplementary explicit training on the nonsense words. Statistical learning was assessed through a speeded reaction-time (RT) task, which measured the extent to which learners used acquired statistical knowledge to optimize online processing. Both RTs and brain potentials revealed significant differences in online processing as a function of training condition. RTs showed a crossover interaction; responses in the explicit group were faster to predictable targets and marginally slower to less predictable targets relative to responses in the implicit group. P300 potentials to predictable targets were larger in the explicit group than in the implicit group, suggesting greater recruitment of controlled, effortful processes. Taken together, these results suggest that information abstracted through passive exposure during statistical learning may be processed more automatically and with less effort than information that is acquired explicitly.

Quantifying transfer after perceptual-motor sequence learning: how inflexible is implicit learning?

Studies of implicit perceptual-motor sequence learning have often shown learning to be inflexibly tied to the training conditions during learning. Since sequence learning is seen as a model task of skill acquisition, limits on the ability to transfer knowledge from the training context to a performance context indicates important constraints on skill learning approaches. Lack of transfer across contexts has been demonstrated by showing that when task elements are changed following training, this leads to a disruption in performance. These results have typically been taken as suggesting that the sequence knowledge relies on integrated representations across task elements (Abrahamse, Jiménez, Verwey, & Clegg, Psychon Bull Rev 17:603-623, 2010a). Using a relatively new sequence learning task, serial interception sequence learning, three experiments are reported that quantify this magnitude of performance disruption after selectively manipulating individual aspects of motor performance or perceptual information. In Experiment 1, selective disruption of the timing or order of sequential actions was examined using a novel response manipulandum that allowed for separate analysis of these two motor response components. In Experiments 2 and 3, transfer was examined after selective disruption of perceptual information that left the motor response sequence intact. All three experiments provided quantifiable estimates of partial transfer to novel contexts that suggest some level of information integration across task elements. However, the ability to identify quantifiable levels of successful transfer indicates that integration is not all-or-none and that measurement sensitivity is a key in understanding sequence knowledge representations.

Neural correlates of sexual arousal in heterosexual and homosexual women and men.

Most men have a category-specific pattern of genital and subjective sexual arousal, responding much more strongly to erotic stimuli depicting their preferred sex than to erotic stimuli depicting their nonpreferred sex. In contrast, women tend to have a less specific arousal pattern. To better understand this sex difference, we used neuroimaging to explore its neural correlates. Heterosexual and homosexual women viewed erotic photographs of either men or women. Evoked neural activity was monitored via fMRI and compared with responses to the same stimuli in heterosexual and homosexual men. Overall, a network of limbic (as well as the anterior cingulate) and visual processing regions showed significantly less category-specific activity in women than men. This was primarily driven by weaker overall activations to preferred-sex stimuli in women, though there was also some evidence of stronger limbic activations to nonpreferred-sex stimuli in women. Primary results were similar for heterosexual and homosexual participants. Women did show some evidence of category-specific responses in the visual processing regions, although even in these regions they exhibited less differential activity than men. In the anterior cingulate, a region with high concentrations of sex-hormone receptors, subjective and neural category specificity measures correlated positively for women but negatively for men, suggesting a possible sex difference in the role of the anterior cingulate. Overall, results suggest that men tend to show more differentiated neural responses than do women to erotic photographs of one sex compared to the other sex, though women may not be entirely indifferent to which sex is depicted.

Medial temporal contributions to successful face-name learning.

The brain mechanisms that enable us to form durable associations between different types of information are not completely understood. Although the hippocampus is widely thought to play a substantial role in forming associations, the role of surrounding cortical regions in the medial temporal lobe, including perirhinal and parahippocampal cortex, is controversial. Using anatomically constrained functional magnetic resonance imaging, we assessed medial temporal contributions to learning arbitrary associations between faces and names. By sorting learning trials based on subsequent performance in associative and item-specific memory tests, we characterized brain activity associated with successful face-name associative learning. We found that right hippocampal activity was greater when corresponding face-name associations were subsequently remembered than when only a face or a name, but not both, were remembered, or when single-item information or associative information was not remembered. Neither perirhinal nor parahippocampal cortex encoding activity differed across these same conditions. Furthermore, right hippocampal activity during successful face-name association learning was strongly correlated with activity in cortical regions involved in multimodal integration, supporting the idea that interactions between the hippocampus and neocortex contribute to associative memory. These results specifically implicate the hippocampus in associative memory formation, in keeping with theoretical formulations in which contributions to across-domain binding differ among brain structures in the medial temporal region.

Implicit sequence learning using auditory cues leads to modality-specific representations.

The implicit acquisition of statistical information from the environment is considered a fundamental type of human learning. Paradigms using visually cued sequences have been frequently used to study implicit learning. However, learning sequences of auditory cues is likely to be important in domains such as language or music. In three experiments, we established a novel auditorily cued implicit perceptual-motor sequence learning paradigm to compare to traditional visually cued sequence learning and identify whether this type of learning generalizes across cue modality. Participants exhibited reliable sequence-specific learning to auditory cues in all three experiments (Experiments 1-3), which was generally not influenced by explicit knowledge (Experiment 2). In Experiment 3, a large drop in knowledge expression in the novel cue modality was observed, suggesting that the acquired implicit sequence knowledge depended largely on sensory-specific representations. Overall, auditorily cued learning was similar to, though proceeded faster than, learning in comparable visually cued sequence learning paradigms. Similarity between learning from cues in different sensory modalities suggests that there may be a common process for the automatic extraction of sequential statistical structure. However, the lack of robust transfer sequence knowledge across modalities argues against a purely domain-general learning mechanism for all kinds of sequences. By expanding quantitative methodologies to characterize sequence learning in the auditory domain, these findings illustrate the possibility of bridging research in sequence and statistical learning domains to identify common mechanisms of complex cognitive skill and language learning.

Neural correlates of skill acquisition: decreased cortical activity during a serial interception sequence learning task.

Learning of complex motor skills requires learning of component movements as well as the sequential structure of their order and timing. Using a Serial Interception Sequence Learning (SISL) task, participants learned a sequence of precisely timed interception responses through training with a repeating sequence. Following initial implicit learning of the repeating sequence, functional MRI data were collected during performance of that known sequence and compared with activity evoked during novel sequences of actions, novel timing patterns, or both. Reduced activity was observed during the practiced sequence in a distributed bilateral network including extrastriate occipital, parietal, and premotor cortical regions. These reductions in evoked activity likely reflect improved efficiency in visuospatial processing, spatio-motor integration, motor planning, and motor execution for the trained sequence, which is likely supported by nondeclarative skill learning. In addition, the practiced sequence evoked increased activity in the left ventral striatum and medial prefrontal cortex, while the posterior cingulate was more active during periods of better performance. Many prior studies of perceptual-motor skill learning have found increased activity in motor areas of the frontal cortex (e.g., motor and premotor cortex, SMA) and striatal areas (e.g., the putamen). The change in activity observed here (i.e., decreased activity across a cortical network) may reflect skill learning that is predominantly expressed through more accurate performance rather than decreased reaction time.

Familiarity and conceptual priming engage distinct cortical networks.

Familiarity refers to an explicit recognition experience without any necessary retrieval of specific detail related to the episode during which initial learning transpired. Prior experience can also implicitly influence subsequent processing through a memory phenomenon termed conceptual priming, which occurs without explicit awareness of recognition. Resolving current theoretical controversy on relationships between familiarity and conceptual priming requires a clarification of their neural substrates. Accordingly, we obtained functional magnetic resonance images in a novel paradigm for separately assessing neural correlates of familiarity and conceptual priming using famous and nonfamous faces. Conceptual priming, as shown by more accurate behavioral responses to strongly conceptually primed than to weakly conceptually primed faces, was associated with activity reductions in left prefrontal cortex, whereas familiarity was associated with activity enhancements in right parietal cortex for more-familiar compared with less-familiar faces. This neuroimaging evidence implicates separate neurocognitive processes operative in explicit stimulus recognition versus implicit conceptual priming.

Understanding the Neural Bases of Implicit and Statistical Learning.

Both implicit learning and statistical learning focus on the ability of learners to pick up on patterns in the environment. It has been suggested that these two lines of research may be combined into a single construct of "implicit statistical learning." However, by comparing the neural processes that give rise to implicit versus statistical learning, we may determine the extent to which these two learning paradigms do indeed describe the same core mechanisms. In this review, we describe current knowledge about neural mechanisms underlying both implicit learning and statistical learning, highlighting converging findings between these two literatures. A common thread across all paradigms is that learning is supported by interactions between the declarative and nondeclarative memory systems of the brain. We conclude by discussing several outstanding research questions and future directions for each of these two research fields. Moving forward, we suggest that the two literatures may interface by defining learning according to experimental paradigm, with "implicit learning" reserved as a specific term to denote learning without awareness, which may potentially occur across all paradigms. By continuing to align these two strands of research, we will be in a better position to characterize the neural bases of both implicit and statistical learning, ultimately improving our understanding of core mechanisms that underlie a wide variety of human cognitive abilities.

Motivation to avoid loss improves implicit skill performance.

Implicit learning reflects learning from experience that occurs without intention or awareness of the information acquired and is hypothesized to contribute to skill acquisition by improving performance with practice. The role of motivation has not been examined because this kind of memory is represented outside awareness. We manipulated motivation (approach/avoidance) and type of feedback (positive/negative) to measure how these affected a well-studied task of implicit sequence learning. Across 2 experiments, we found a consistent effect that motivation to avoid loss led to much higher levels of sequence-specific task performance. When the motivation manipulation was removed, performance fell to typical levels, indicating that motivation enhanced knowledge expression through performance, not learning. Even though implicit skill knowledge is represented outside awareness, our ability to apply this knowledge is enhanced when motivated by fear of loss, potentially providing insight into the value of coaching/training practices that motivate performers in this manner. (PsycINFO Database Record

Neural correlates of sexual arousal in homosexual and heterosexual men.

Men exhibit much higher levels of genital and subjective arousal to sexual stimuli containing their preferred sex than they do to stimuli containing only the nonpreferred sex. This study used event-related functional magnetic resonance imaging to investigate how this category-specific pattern would be reflected in the brains of homosexual (n = 11) and heterosexual (n = 11) men. Comparisons of activation to preferred sexual stimuli, nonpreferred sexual stimuli, and sports stimuli revealed large networks correlated with sexual arousal, spanning multiple cortical and subcortical areas. Both homosexual and heterosexual men exhibited category-specific arousal in brain activity. Within the amygdala, greater preference-related activity was observed in homosexual men, but it is unclear whether this is a cause or a consequence of their sexuality. In a subsequent analysis of regions hypothesized to support arousal, both participant groups demonstrated widespread increases in evoked activity for preferred stimuli. Aggregate data from these regions produced significant differences between stimulus types in 16 out of 22 participants. Significant activational differences matched reported sexual orientation in 15 of these 16 participants, representing an advance in psychophysiological measures of arousal.

Neural activity when people solve verbal problems with insight.

People sometimes solve problems with a unique process called insight, accompanied by an "Aha!" experience. It has long been unclear whether different cognitive and neural processes lead to insight versus noninsight solutions, or if solutions differ only in subsequent subjective feeling. Recent behavioral studies indicate distinct patterns of performance and suggest differential hemispheric involvement for insight and noninsight solutions. Subjects solved verbal problems, and after each correct solution indicated whether they solved with or without insight. We observed two objective neural correlates of insight. Functional magnetic resonance imaging (Experiment 1) revealed increased activity in the right hemisphere anterior superior temporal gyrus for insight relative to noninsight solutions. The same region was active during initial solving efforts. Scalp electroencephalogram recordings (Experiment 2) revealed a sudden burst of high-frequency (gamma-band) neural activity in the same area beginning 0.3 s prior to insight solutions. This right anterior temporal area is associated with making connections across distantly related information during comprehension. Although all problem solving relies on a largely shared cortical network, the sudden flash of insight occurs when solvers engage distinct neural and cognitive processes that allow them to see connections that previously eluded them.

When memory does not fail: familiarity-based recognition in mild cognitive impairment and Alzheimer's disease.

Recognition can be guided by familiarity, a restricted form of retrieval devoid of contextual recall, or by recollection, which occurs when retrieval is sufficient to support the full experience of remembering an episode. Recollection and familiarity were disentangled by testing recognition memory using silhouette object drawings, high target-foil resemblance, and both yes-no and forced-choice procedures. Theoretically, forced-choice recognition could be mediated by familiarity alone. Alzheimer's disease and its preclinical stage, mild cognitive impairment (MCI), were associated with memory impairments that were greater on the yes-no test. Remarkably, forced-choice recognition was unequivocally normal in patients with MCI compared with age-matched controls. Neuropathology in hippocampus and entorhinal cortex, known to be present in MCI, presumably disrupted recollection while leaving familiarity-based recognition intact.

Compensatory processing during rule-based category learning in older adults.

Healthy older adults typically perform worse than younger adults at rule-based category learning, but better than patients with Alzheimer's or Parkinson's disease. To further investigate aging's effect on rule-based category learning, we monitored event-related potentials (ERPs) while younger and neuropsychologically typical older adults performed a visual category-learning task with a rule-based category structure and trial-by-trial feedback. Using these procedures, we previously identified ERPs sensitive to categorization strategy and accuracy in young participants. In addition, previous studies have demonstrated the importance of neural processing in the prefrontal cortex and the medial temporal lobe for this task. In this study, older adults showed lower accuracy and longer response times than younger adults, but there were two distinct subgroups of older adults. One subgroup showed near-chance performance throughout the procedure, never categorizing accurately. The other subgroup reached asymptotic accuracy that was equivalent to that in younger adults, although they categorized more slowly. These two subgroups were further distinguished via ERPs. Consistent with the compensation theory of cognitive aging, older adults who successfully learned showed larger frontal ERPs when compared with younger adults. Recruitment of prefrontal resources may have improved performance while slowing response times. Additionally, correlations of feedback-locked P300 amplitudes with category-learning accuracy differentiated successful younger and older adults. Overall, the results suggest that the ability to adapt one's behavior in response to feedback during learning varies across older individuals, and that the failure of some to adapt their behavior may reflect inadequate engagement of prefrontal cortex.

Neural correlates of successful encoding identified using functional magnetic resonance imaging.

Neural activity that occurs during the creation of a new memory trace can be observed using functional magnetic resonance imaging (fMRI). Event-related designs have been used to demonstrate that activity in prefrontal and medial temporal lobe areas is associated with successful memory storage. Here we contrasted activity associated with encoding success and encoding effort. Participants viewed a series of 150 words but attempted to remember only half of them. Encoding effort was manipulated using a cue in the form of a letter (R or F) presented after each word to instruct participants either to remember or to forget that word. Increased activity in left inferior prefrontal cortex was observed when words were followed by the cue to remember. In contrast, increased left medial temporal lobe activity was observed for words that were successfully recalled later. These results show that fMRI correlates of the intention to encode a word are different from fMRI correlates of whether that encoding is successful. Prefrontal activation was strongly associated with intentional verbal encoding, whereas left medial temporal activation was crucial for the encoding that actually led to successful memory on the subsequent test.

Implicit and explicit contributions to statistical learning.

Statistical learning allows learners to detect regularities in the environment and appears to emerge automatically as a consequence of experience. Statistical learning paradigms bear many similarities to those of artificial grammar learning and other types of implicit learning. However, whether learning effects in statistical learning tasks are driven by implicit knowledge has not been thoroughly examined. The present study addressed this gap by examining the role of implicit and explicit knowledge within the context of a typical auditory statistical learning paradigm. Learners were exposed to a continuous stream of repeating nonsense words. Learning was tested (a) directly via a forced-choice recognition test combined with a remember/know procedure and (b) indirectly through a novel reaction time (RT) test. Behavior and brain potentials revealed statistical learning effects with both tests. On the recognition test, accurate responses were associated with subjective feelings of stronger recollection, and learned nonsense words relative to nonword foils elicited an enhanced late positive potential indicative of explicit knowledge. On the RT test, both RTs and P300 amplitudes differed as a function of syllable position, reflecting facilitation attributable to statistical learning. Explicit stimulus recognition did not correlate with RT or P300 effects on the RT test. These results provide evidence that explicit knowledge is accrued during statistical learning, while bringing out the possibility that dissociable implicit representations are acquired in parallel. The commonly used recognition measure primarily reflects explicit knowledge, and thus may underestimate the total amount of knowledge produced by statistical learning. Indirect measures may be more sensitive indices of learning, capturing knowledge above and beyond what is reflected by recognition accuracy.

Dissociation of category-learning systems via brain potentials.

Behavioral, neuropsychological, and neuroimaging evidence has suggested that categories can often be learned via either an explicit rule-based (RB) mechanism critically dependent on medial temporal and prefrontal brain regions, or via an implicit information-integration (II) mechanism relying on the basal ganglia. In this study, participants viewed sine-wave gratings (Gabor patches) that varied on two dimensions and learned to categorize them via trial-by-trial feedback. Two different stimulus distributions were used; one was intended to encourage an explicit RB process and the other an implicit II process. We monitored brain activity with scalp electroencephalography (EEG) while each participant: (1) passively observed stimuli represented of both distributions; (2) categorized stimuli from one distribution, and, 1 week later; (3) categorized stimuli from the other distribution. Categorization accuracy was similar for the two distributions. Subtractions of Event-Related Potentials (ERPs) for correct and incorrect trials were used to identify neural differences in RB and II categorization processes. We identified an occipital brain potential that was differentially modulated by categorization condition accuracy at an early latency (150-250 ms), likely reflecting the degree of holistic processing. A stimulus-locked Late Positive Complex (LPC) associated with explicit memory updating was modulated by accuracy in the RB, but not the II task. Likewise, a feedback-locked P300 ERP associated with expectancy was correlated with performance only in the RB, but not the II condition. These results provide additional evidence for distinct brain mechanisms supporting RB vs. implicit II category learning and use.

Benefits of mindfulness training for patients with progressive cognitive decline and their caregivers.

New strategies are needed to help people cope with the repercussions of neurodegenerative disorders such as Alzheimer's disease. Patients and caregivers face different challenges, but here we investigated an intervention tailored for this combined population. The program focused on training skills such as attending to the present moment nonjudgmentally, which may help reduce maladaptive emotional responses. Patients participated together with caregivers in weekly group sessions over 8 weeks. An assessment battery was individually administered before and after the program. Pre-post analyses revealed several benefits, including increased quality-of-life ratings, fewer depressive symptoms, and better subjective sleep quality. In addition, participants indicated that they were grateful for the opportunity to learn to apply mindfulness skills and that they would recommend the program to others. In conclusion, mindfulness training can be beneficial for patients and their caregivers, it can be delivered at low cost to combined groups, and it is worthy of further investigation.