Task-related functional connectivity of the caudate mediates the association between trait mindfulness and implicit learning in older adults.

Accumulating evidence shows a positive relationship between mindfulness and explicit cognitive functioning, i.e., that which occurs with conscious intent and awareness. However, recent evidence suggests that there may be a negative relationship between mindfulness and implicit types of learning, or those that occur without conscious awareness or intent. Here we examined the neural mechanisms underlying the recently reported negative relationship between dispositional mindfulness and implicit probabilistic sequence learning in both younger and older adults. We tested the hypothesis that the relationship is mediated by communication, or functional connectivity, of brain regions once traditionally considered to be central to dissociable learning systems: the caudate, medial temporal lobe (MTL), and prefrontal cortex (PFC). We first replicated the negative relationship between mindfulness and implicit learning in a sample of healthy older adults (60-90 years old) who completed three event-related runs of an implicit sequence learning task. Then, using a seed-based connectivity approach, we identified task-related connectivity associated with individual differences in both learning and mindfulness. The main finding was that caudate-MTL connectivity (bilaterally) was positively correlated with learning and negatively correlated with mindfulness. Further, the strength of task-related connectivity between these regions mediated the negative relationship between mindfulness and learning. This pattern of results was limited to the older adults. Thus, at least in healthy older adults, the functional communication between two interactive learning-relevant systems can account for the relationship between mindfulness and implicit probabilistic sequence learning.

Relationship of contextual cueing and hippocampal volume in amnestic mild cognitive impairment patients and cognitively normal older adults.

There is currently some debate as to whether hippocampus mediates contextual cueing. In the present study, we examined contextual cueing in patients diagnosed with mild cognitive impairment (MCI) and healthy older adults, with the main goal of investigating the role of hippocampus in this form of learning. Amnestic MCI (aMCI) patients and healthy controls completed the contextual cueing task, in which they were asked to search for a target (a horizontal T) in an array of distractors (rotated L's). Unbeknownst to them, the spatial arrangement of elements on some displays was repeated thus making the configuration a contextual cue to the location of the target. In contrast, the configuration for novel displays was generated randomly on each trial. The difference in response times between repeated and novel configurations served as a measure of contextual learning. aMCI patients, as a group, were able to learn spatial contextual cues as well as healthy older adults. However, better learning on this task was associated with higher hippocampal volume, particularly in right hemisphere. Furthermore, contextual cueing performance was significantly associated with hippocampal volume, even after controlling for age and MCI status. These findings support the role of the hippocampus in learning of spatial contexts, and also suggest that the contextual cueing paradigm can be useful in detecting neuropathological changes associated with the hippocampus.

Effects of priming goal pursuit on implicit sequence learning.

Implicit learning, the type of learning that occurs without intent to learn or awareness of what has been learned, has been thought to be insensitive to the effects of priming, but recent studies suggest this is not the case. One study found that learning in the serial reaction time (SRT) task was improved by nonconscious goal pursuit, primed via a word search task (Eitam et al. in Psychol Sci 19:261-267, 2008). In two studies, we used the goal priming word search task from Eitam et al., but with a different version of the SRT, the alternating serial reaction time task (ASRT). Unlike the SRT, which often results in explicit knowledge and assesses sequence learning at one point in time, the ASRT has been shown to be implicit through sensitive measures of judgment, and it enables sequence learning to be measured continuously. In both studies, we found that implicit learning was superior in the groups that were primed for goal achievement compared to control groups, but the effect was transient. We discuss possible reasons for the observed time course of the positive effects of goal priming, as well as some future areas of investigation to better understand the mechanisms that underlie this effect, which could lead to methods to prolong the positive effects.

Dispositional mindfulness is associated with reduced implicit learning.

Behavioral and neuroimaging evidence suggest that mindfulness exerts its salutary effects by disengaging habitual processes supported by subcortical regions and increasing effortful control processes supported by the frontal lobes. Here we investigated whether individual differences in dispositional mindfulness relate to performance on implicit sequence learning tasks in which optimal learning may in fact be impeded by the engagement of effortful control processes. We report results from two studies where participants completed a widely used questionnaire assessing mindfulness and one of two implicit sequence learning tasks. Learning was quantified using two commonly used measures of sequence learning. In both studies we detected a negative relationship between mindfulness and sequence learning, and the relationship was consistent across both learning measures. Our results, the first to show a negative relationship between mindfulness and implicit sequence learning, suggest that the beneficial effects of mindfulness do not extend to all cognitive functions.

The effects of healthy aging on the mnemonic benefit of survival processing.

A number of studies have shown that information is remembered better when it is processed for its survival relevance than when it is processed for relevance to other, non-survival-related contexts. Here we conducted three experiments to investigate whether the survival advantage also occurs for healthy older adults. In Experiment 1, older and younger adults rated words for their relevance to a grassland survival or moving scenario and then completed an unexpected free recall test on the words. We replicated the survival advantage in two separate groups of younger adults, one of which was placed under divided-attention conditions, but we did not find a survival advantage in the older adults. We then tested two additional samples of older adults using a between- (Exp. 2) or within- (Exp. 3) subjects design, but still found no evidence of the survival advantage in this age group. These results suggest that, although survival processing is an effective encoding strategy for younger adults, it does not provide the same mnemonic benefit to healthy elders.

Not just scenery: viewing nature pictures improves executive attention in older adults.

UNLABELLED: BACKGROUND/STUDY CONTEXT: Attention Restoration Theory (Kaplan, 1995, Journal of Environmental Psychology, 15, 169-182) suggests that exposure to nature improves attention. Berman, Jonides, and Kaplan (2008, Psychological Science, 19, 1207-1212) showed that simply viewing nature pictures improves executive attention in young adults. The present study is the first to investigate this Nature Effect in older adults. The authors investigated whether executive attention could be improved in healthy older adults following brief exposure to nature pictures. METHODS: Thirty healthy older adults (64-79 years old) and 26 young university students (18-25 years old) participated. They completed the Attention Network Test before and after 6 min of viewing either nature or urban pictures, with random assignment into a picture type. Attention immediately before (most fatigued) and after (most restored) picture viewing was measured, and change in attention was compared between age groups and picture types. RESULTS: Results showed that viewing nature, but not urban, pictures significantly improved executive attention in both older and young adults as measured by the Attention Network Test, with similar effects seen in the two age groups. Alerting and orienting attention scores were not affected by picture viewing. CONCLUSION: This was the first study to show that viewing nature pictures improves attention in older adults, and to show that it is executive attention, specifically, that is improved. Among a growing number of interventions, nature exposure offers a quick, inexpensive, and enjoyable means to provide a temporary boost in executive attention.

The effects of aging on the neural basis of implicit associative learning in a probabilistic triplets learning task.

Few studies have investigated how aging influences the neural basis of implicit associative learning, and available evidence is inconclusive. One emerging behavioral pattern is that age differences increase with practice, perhaps reflecting the involvement of different brain regions with training. Many studies report hippocampal involvement early on with learning becoming increasingly dependent on the caudate with practice. We tested the hypothesis that the contribution of these regions to learning changes with age because of differential age-related declines in the striatum and hippocampi. We assessed age-related differences in brain activation during implicit associative learning using the Triplets Learning Task. Over three event-related fMRI runs, 11 younger and 12 healthy older adults responded to only the third (target) stimulus in sequences of three stimuli ("triplets") by corresponding key press. Unbeknown to participants, the first stimulus' location predicted one target location for 80% of trials and another target location for 20% of trials. Both age groups learned associative regularities but differences in favor of the younger adults emerged with practice. The neural basis of learning (response to predictability) was examined by identifying regions that showed a greater response to triplets that occurred more frequently. Both age groups recruited the hippocampus early, but with training, the younger adults recruited their caudate whereas the older adults continued to rely on their hippocampus. This pattern enables older adults to maintain near-young levels of performance early in training, but not later, and adds to evidence that implicit associative learning is supported by different brain networks in younger and older adults.

Age-related differences in multiple measures of white matter integrity: A diffusion tensor imaging study of healthy aging.

Diffusion tensor imaging (DTI) measures diffusion of molecular water, which can be used to calculate indices of white matter integrity. Early DTI studies of aging primarily focused on two global measures of integrity; the average rate (mean diffusivity, MD) and orientation coherence (fractional anisotropy, FA) of diffusion. More recent studies have added measures of water movement parallel (axial diffusivity, AD) and perpendicular (radial diffusivity, RD) to the primary diffusion direction, which are thought to reflect the neural bases of age differences in diffusion (i.e., axonal shrinkage and demyelination, respectively). In this study, patterns of age differences in white matter integrity were assessed by comparing younger and healthy older adults on multiple measures of integrity (FA, AD, and RD). Results revealed two commonly reported patterns (Radial Increase Only and Radial/Axial Increase), and one relatively novel pattern (Radial Increase/Axial Decrease) that varied by brain region and may reflect differential aging of microstructural (e.g., degree of myelination) and macrostructural (e.g., coherence of fiber orientation) properties of white matter. In addition, larger age differences in FA in frontal white matter were consistent with the anterior-posterior gradient of age differences in white matter integrity. Together, these findings complement other recent studies in providing information about patterns of diffusivity that are characteristic of healthy aging.

Sleep has no critical role in implicit motor sequence learning in young and old adults.

The influence of sleep on motor skill consolidation has been a research topic of increasing interest. In this study, we distinguished general skill learning from sequence-specific learning in a probabilistic implicit sequence learning task (alternating serial reaction time) in young and old adults before and after a 12-h offline interval which did or did not contain sleep (p.m.-a.m. and a.m.-p.m. groups, respectively). The results showed that general skill learning, as assessed via overall reaction time, improved offline in both the young and older groups, with the young group improving more than the old. However, the improvement was not sleep-dependent, in that there was no difference between the a.m.-p.m. and p.m.-a.m. groups. We did not find sequence-specific offline improvement in either age group for the a.m.-either p.m. or p.m.-a.m. groups, suggesting that consolidation of this kind of implicit motor sequence learning may not be influenced by sleep.

One-year retention of general and sequence-specific skills in a probabilistic, serial reaction time task.

Procedural skills such as riding a bicycle and playing a musical instrument play a central role in daily life. Such skills are learned gradually and are retained throughout life. The present study investigated 1-year retention of procedural skill in a version of the widely used serial reaction time task (SRTT) in young and older motor-skill experts and older controls in two experiments. The young experts were college-age piano and action video-game players, and the older experts were piano players. Previous studies have reported sequence-specific skill retention in the SRTT as long as 2 weeks but not at 1 year. Results indicated that both young and older experts and older non-experts revealed sequence-specific skill retention after 1 year with some evidence that general motor skill was retained as well. These findings are consistent with theoretical accounts of procedural skill learning such as the procedural reinstatement theory as well as with previous studies of retention of other motor skills.

Sleep does not benefit probabilistic motor sequence learning.

It has become widely accepted that sleep-dependent consolidation occurs for motor sequence learning based on studies using finger-tapping tasks. Studies using another motor sequence learning task [the serial response time task (SRTT)] have portrayed a more nuanced picture of off-line consolidation, involving both sleep-dependent and daytime consolidation, as well as modifying influences of explicit awareness. The present study used a variant of the SRTT featuring probabilistic sequences to investigate off-line consolidation. Probabilistic sequences confer two advantages: first, spontaneous explicit awareness does not occur, and second, sequence learning measures are continuous, making it easier to separate general skill from sequence-specific learning. We found that sleep did not enhance general skill or sequence-specific learning. In contrast, daytime enhancement occurred for general skill but not for sequence-specific learning. Overall, these results suggest that motor learning does not always undergo consolidation with sleep.

Intact implicit learning of spatial context and temporal sequences in childhood autism spectrum disorder.

Autism spectrum disorder (ASD) is defined by atypicalities in domains that are posited to rely on implicit learning processes such as social communication, language, and motor behavior. The authors examined 2 forms of implicit learning in 14 children with high-functioning ASD (10 of whom were diagnosed with Asperger's syndrome) and 14 control children, learning of spatial context known to be mediated by the medial temporal lobes (using the contextual cueing task) and of sequences known to be mediated by frontal-striatal and frontal-cerebellar circuits (using the alternating serial reaction time task). Both forms of learning were unimpaired in ASD. Spatial contextual implicit learning was spared in ASD despite slower visual search of spatial displays. The present findings provide evidence for the integrity of learning processes dependent on integration of spatial and sequential contextual information in high-functioning children with ASD.

Perceptual sequence learning in a serial reaction time task.

In the serial reaction time task (SRTT), a sequence of visuo-spatial cues instructs subjects to perform a sequence of movements which follow a repeating pattern. Though motor responses are known to support implicit sequence learning in this task, the goal of the present experiments is to determine whether observation of the sequence of cues alone can also yield evidence of implicit sequence learning. This question has been difficult to answer because in previous research, performance improvements which appeared to be due to implicit perceptual sequence learning could also be due to spontaneous increases in explicit knowledge of the sequence. The present experiments use probabilistic sequences to prevent the spontaneous development of explicit awareness. They include a training phase, during which half of the subjects observe and the other half respond, followed by a transfer phase in which everyone responds. Results show that observation alone can support sequence learning, which translates at transfer into equivalent performance as that of a group who made motor responses during training. However, perceptual learning or its expression is sensitive to changes in target colors, and its expression is impaired by concurrent explicit search. Motor-response based learning is not affected by these manipulations. Thus, observation alone can support implicit sequence learning, even of higher order probabilistic sequences. However, perceptual learning can be prevented or concealed by variations of stimuli or task demands.

Implicit learning of predictive relationships in three-element visual sequences by young and old adults.

Knowledge of sequential relationships enables future events to be anticipated and processed efficiently. Research with the serial reaction time task (SRTT) has shown that sequence learning often occurs implicitly without effort or awareness. Here, the authors report 4 experiments that use a triplet-learning task (TLT) to investigate sequence learning in young and older adults. In the TLT, people respond only to the last target event in a series of discrete, 3-event sequences or triplets. Target predictability is manipulated by varying the triplet frequency (joint probability) and/or the statistical relationships (conditional probabilities) among events within the triplets. Results reveal that both groups learned, though older adults showed less learning of both joint and conditional probabilities. Young people used the statistical information in both cues, but older adults relied primarily on information in the 2nd cue alone. The authors conclude that the TLT complements and extends the SRTT and other tasks by offering flexibility in the kinds of sequential statistical regularities that may be studied as well as by controlling event timing and eliminating motor response sequencing.

Aging and implicit learning of an invariant association.

We investigated whether there is an age-related decline in implicit learning of an invariant association. Participants memorized letter strings in which a given letter always occurred in the second position (see Frick & Lee, 1995). Experiments 1 and 2 showed that young and older adults learned this regularity implicitly, with no significant age differences, even when a perceptual feature of the stimuli changed between encoding and test. Experiment 3 confirmed that learning had occurred during encoding, in that learning increased with the number of encoding presentations. We conclude that implicit learning of this invariant association is largely preserved in healthy aging, revealing another avenue by which older people continue to adapt efficiently to environmental regularities.

Implicit probabilistic sequence learning is independent of explicit awareness.

Studies into interactions between explicit and implicit motor sequence learning have yielded mixed results. Some of these discrepancies have been attributed to difficulties in isolating implicit learning. In the present study, the effect of explicit knowledge on implicit learning was investigated using a modified version of the Alternating Serial Response Time (ASRT) task, a probabilistic sequence learning paradigm that yields continuous and relatively pure measures of implicit learning. Results revealed that implicit learning occurred to the same extent, whether or not subjects had explicit knowledge. Some evidence, however, indicated that explicit knowledge could interfere with the expression of implicit learning early in training. In addition, there were dissociations between learning measures, in that reaction time and accuracy were differentially affected by explicit knowledge. These findings indicate that implicit sequence learning occurs independently of explicit knowledge, and help to explain previous discrepant findings.

Developmental differences in implicit learning of spatial context.

The authors examined whether a form of implicit memory that has been unambiguously dissociated from conscious awareness--learning of spatial context on the contextual cuing task introduced by M. M. Chun and Y. Jiang (1998)--is mature in childhood as predicted by an evolutionary view of cognition. School-aged children did not show reliable learning relative to adults who performed the same version of the task or another version that slowed responses to match those of children. Thus, unreliable learning in childhood was mediated by immature implicit representations of spatial context rather than by slower baseline response speed. The present finding is inconsistent with the prediction of the evolutionary view of cognition but consistent with incomplete maturation of medial temporal lobes known to mediate contextual learning.

Age-related differences in implicit learning of subtle third-order sequential structure.

Age-related implicit learning deficits increase with sequence complexity, suggesting there might be limits to the level of structure that older adults can learn implicitly. To test for such limits, we had 12 younger and 12 older adults complete an alternating serial reaction time task containing subtle structure in which every third trial follows a repeating sequence and intervening trials are determined randomly. Results revealed significant age deficits in learning. However, both groups did learn the subtle regularity without explicit awareness, indicating that older adults remain sensitive to highly complex sequential regularities in their environment, albeit to a lesser degree than younger adults.

Event Timing and age deficits in higher-order sequence learning.

Recent studies have reported age deficits in learning sequences that contain subtle sequential regularities (e.g., Curran (1997) Psychological Research, 60(1-2), 24; D. V. Howard et al. (2004) Psychology and Aging, 19(1), 79; Howard, J. H. Jr, & Howard, D. V. (1997). Psychology and Aging, 12(4), 634). This finding is of potential theoretical interest, but the contribution of sequence event timing to this deficit has not been investigated. This study used an alternating serial reaction time task to examine implicit sequence learning in young adults when event timing mimicked that experienced by older adults in previous research. We varied the response-to-stimulus interval directly in Experiment 1 and indirectly by degrading the stimuli to influence response time in Experiment 2. Results indicate that these "aged" young adults learned the higher-order sequence structure implicitly, but they learned less than young controls and more than old adults on some measures of implicit learning in both experiments. In addition, these two different experimental manipulations produced distinct patterns of deficits despite having nearly identical effects on event sequence timing. These findings suggest that event timing alone cannot explain the age deficits observed in high-order implicit sequence learning.

Individual Differences in Cognitive Function in Older Adults Predicted by Neuronal Selectivity at Corresponding Brain Regions.

Relating individual differences in cognitive abilities to neural substrates in older adults is of significant scientific and clinical interest, but remains a major challenge. Previous functional magnetic resonance imaging (fMRI) studies of cognitive aging have mainly focused on the amplitude of fMRI response, which does not measure neuronal selectivity and has led to some conflicting findings. Here, using local regional heterogeneity analysis, or Hcorr , a novel fMRI analysis technique developed to probe the sparseness of neuronal activations as an indirect measure of neuronal selectivity, we found that individual differences in two different cognitive functions, episodic memory and letter verbal fluency, are selectively related to Hcorr -estimated neuronal selectivity at their corresponding brain regions (hippocampus and visual-word form area, respectively). This suggests a direct relationship between cognitive function and neuronal selectivity at the corresponding brain regions in healthy older adults, which in turn suggests that age-related neural dedifferentiation might contribute to rather than compensate for cognitive decline in healthy older adults. Additionally, the capability to estimate neuronal selectivity across brain regions with a single data set and link them to cognitive performance suggests that, compared to fMRI-adaptation-the established fMRI technique to assess neuronal selectivity, Hcorr might be a better alternative in studying normal aging and neurodegenerative diseases, both of which are associated with widespread changes across the brain.