ABSTRACT
Classical lesion studies led to a consensus that episodic and procedural memory arises from segregated networks identified with the hippocampus and the caudate nucleus, respectively. Neuroimaging studies, however, show that competitive and cooperative interactions occur between networks during memory tasks. Furthermore, causal experiments to manipulate connectivity between these networks have not been performed in humans. Although nodes common to both networks, such as the precuneus and ventrolateral thalamus, may mediate their interaction, there is no experimental evidence for this. We tested how network-targeted noninvasive brain stimulation affects episodic-procedural network interactions and how these network manipulations affect episodic and procedural memory in healthy young adults. Compared to control (vertex) stimulation, hippocampal network-targeted stimulation increased within-network functional connectivity and hippocampal connectivity with the caudate. It also increased episodic, relative to procedural, memory, and this persisted one week later. The differential effect on episodic versus procedural memory was associated with increased functional connectivity between the caudate, precuneus, and ventrolateral thalamus. These findings provide direct evidence of episodic-procedural network competition, mediated by regions common to both networks. Enhanced hippocampal network connectivity may boost episodic, but decrease procedural, memory by co-opting resources shared between networks.
Subject(s)
Memory, Episodic , Young Adult , Humans , Magnetic Resonance Imaging , Parietal Lobe/physiology , Hippocampus/physiology , NeuroimagingABSTRACT
Hemispatial neglect is thought to result from disruption of interhemispheric equilibrium. Right hemisphere lesions deactivate the right frontoparietal network and hyperactivate the left via release from interhemispheric inhibition. Support for this putative mechanism comes from neuropsychological evidence as well as transcranial magnetic stimulation (TMS) studies in healthy subjects, in whom right posterior parietal cortex (PPC) inhibition causes neglect-like, rightward, visuospatial bias. Concurrent TMS and fMRI after right PPC TMS show task-dependent changes but may fail to identify effects of stimulation in areas not directly activated by the specific task, complicating interpretations. We used resting-state functional connectivity (RSFC) after inhibitory TMS over the right PPC to examine changes in the networks underlying visuospatial attention and used diffusion-weighted imaging to measure the structural properties of relevant white matter pathways. In a crossover experiment in healthy individuals, we delivered continuous theta burst TMS to the right PPC and vertex as control condition. We hypothesized that PPC inhibitory stimulation would result in a rightward visuospatial bias, decrease frontoparietal RSFC, and increase the PPC RSFC with the attentional network in the left hemisphere. We also expected that individual differences in fractional anisotropy (FA) of the frontoparietal network and the callosal pathway between the PPCs would account for variability of the TMS-induced RSFC changes. As hypothesized, TMS over the right PPC caused a rightward shift in line bisection judgment and increased RSFC between the right PPC and the left superior temporal gyrus. This effect was inversely related to FA in the posterior corpus callosum. Local inhibition of the right PPC reshapes connectivity in the attentional network and depends significantly on interhemispheric connections.
Subject(s)
Attention/physiology , Corpus Callosum/diagnostic imaging , Nerve Net/diagnostic imaging , Perceptual Disorders/diagnostic imaging , Space Perception/physiology , Adult , Anisotropy , Brain Mapping , Corpus Callosum/physiopathology , Female , Functional Laterality/physiology , Humans , Magnetic Resonance Imaging , Male , Nerve Net/physiopathology , Perceptual Disorders/physiopathology , Photic Stimulation , Transcranial Magnetic Stimulation , Young AdultABSTRACT
Repetitive transcranial magnetic stimulation (rTMS) of the inferior parietal cortex (IPC) increases resting-state functional connectivity (rsFC) of the hippocampus with the precuneus and other posterior cortical areas and causes proportional improvement of episodic memory. The anatomical pathway(s) responsible for the propagation of these effects from the IPC is unknown and may not be direct. In order to assess the relative contributions of candidate pathways from the IPC to the MTL via the parahippocampal cortex and precuneus, to the effects of rTMS on rsFC and memory improvement, we used diffusion tensor imaging to measure the extent to which individual differences in fractional anisotropy (FA) in these pathways accounted for individual differences in response. FA in the IPC-parahippocampal pathway and several MTL pathways predicted changes in rsFC. FA in both parahippocampal and hippocampal pathways was related to changes in episodic, but not procedural, memory. These results implicate pathways to the MTL in the enhancing effect of parietal rTMS on hippocampal rsFC and memory.
Subject(s)
Connectome , Hippocampus , Magnetic Resonance Imaging , Memory, Episodic , Nerve Net , Parahippocampal Gyrus , Parietal Lobe , Transcranial Magnetic Stimulation , Adult , Diffusion Tensor Imaging , Female , Hippocampus/anatomy & histology , Hippocampus/diagnostic imaging , Hippocampus/physiology , Humans , Individuality , Male , Nerve Net/anatomy & histology , Nerve Net/diagnostic imaging , Nerve Net/physiology , Neural Pathways/anatomy & histology , Neural Pathways/diagnostic imaging , Neural Pathways/physiology , Parahippocampal Gyrus/anatomy & histology , Parahippocampal Gyrus/diagnostic imaging , Parahippocampal Gyrus/physiology , Parietal Lobe/anatomy & histology , Parietal Lobe/diagnostic imaging , Parietal Lobe/physiology , Young AdultABSTRACT
Prism adaptation (PA) alters spatial cognition according to the direction of visual displacement by temporarily modifying sensorimotor mapping. Right-shifting prisms (right PA) improve neglect of left visual field in patients, possibly by decreasing activity in the left hemisphere and increasing it in the right. Left PA shifts attention rightward in healthy individuals by an opposite mechanism. However, functional imaging studies of PA are inconsistent, perhaps because of differing activation tasks. We measured resting-state functional connectivity (RSFC) in healthy individuals before and after PA. When contrasted, right versus left PA decreased RSFC in the spatial navigation network defined by the right posterior parietal cortex (PPC), hippocampus, and cerebellum. Within-PA-direction comparisons showed that right PA increased RSFC in subregions of the PPCs and between the PPCs and the right middle frontal gyrus and left PA decreased RSFC between these regions. Both right and left PA decreased RSFC between the PPCs and bilateral temporal areas. In summary, right PA increases connectivity in the right frontoparietal network and left PA produces essentially opposite effects. Furthermore, right, compared with left, PA modulates RSFC in the right hemisphere navigation network.
Subject(s)
Adaptation, Physiological/physiology , Neural Pathways/physiology , Parietal Lobe/physiology , Space Perception/physiology , Adult , Attention/physiology , Brain/physiology , Female , Humans , MaleABSTRACT
An important component of learning to read is the acquisition of letter-to-sound mappings. The sheer quantity of mappings and many exceptions in opaque languages such as English suggests that children may use a form of statistical learning to acquire them. However, whereas statistical models of reading are item-based, reading instruction typically focuses on rule-based approaches involving small sets of regularities. This discrepancy poses the question of how different groupings of regularities, an unexamined factor of most reading curricula, may affect learning. Exploring the interplay between item statistics and rules, this study investigated how consonant variability, an item-level factor, and the degree of overlap among the to-be-trained vowel strings, a group-level factor, influence learning. English-speaking first graders (Nâ¯=â¯361) were randomly assigned to be trained on vowel sets with high overlap (e.g., EA, AI) or low overlap (e.g., EE, AI); this was crossed with a manipulation of consonant frame variability. Whereas high vowel overlap led to poorer initial performance, it resulted in more learning when tested immediately and after a 2-week-delay. There was little beneficial effect of consonant variability. These findings indicate that online letter/sound processing affects how new knowledge is integrated into existing information. Moreover, they suggest that vowel overlap should be considered when designing reading curricula.
Subject(s)
Practice, Psychological , Reading , Retention, Psychology/physiology , Child , Female , Humans , Male , Probability Learning , Random AllocationABSTRACT
OBJECTIVE: Repetitive transcranial magnetic stimulation (rTMS) can cause potentially useful changes in brain functional connectivity (FC), but the number of treatment sessions required is unknown. We applied the continual reassessment method (CRM), a Bayesian, adaptive, dose-finding procedure to a rTMS paradigm in an attempt to answer this question. MATERIALS AND METHODS: The sample size was predetermined at 15 subjects and the cohort size was set with three individuals (i.e., five total cohorts). In a series of consecutive daily sessions, we delivered rTMS to the left posterior parietal cortex and measured resting-state FC with fMRI in a predefined hippocampal network in the left hemisphere. The session number for each successive cohort was determined by the CRM algorithm. We set a response criterion of a 0.028 change in FC between the hippocampus and the parietal cortex, which was equal to the increase seen in 87.5% of participants in a previous study using five sessions. RESULTS: A ≥criterion change was observed in 9 of 15 participants. The CRM indicated that greater than four sessions are required to produce the criterion change reliably in future studies. CONCLUSIONS: The CRM can be adapted for rTMS dose finding when a reliable outcome measure, such as FC, is available. The minimum effective dose needed to produce a criterion increase in FC in our hippocampal network of interest at 87.5% efficacy was estimated to be greater than four sessions. This study is the first demonstration of a Bayesian, adaptive method to explore a rTMS parameter.
Subject(s)
Algorithms , Cerebral Cortex/physiology , Hippocampus/physiology , Nerve Net/physiology , Transcranial Magnetic Stimulation/methods , Adult , Female , Humans , Image Processing, Computer-Assisted/methods , Magnetic Resonance Imaging , Male , Neural Pathways/physiology , Pilot ProjectsABSTRACT
Parkinson's disease (PD) is associated with procedural learning deficits. Nonetheless, studies have demonstrated that reward-related learning is comparable between patients with PD and controls (Bódi et al., Brain, 132(9), 2385-2395, 2009; Frank, Seeberger, & O'Reilly, Science, 306(5703), 1940-1943, 2004; Palminteri et al., Proceedings of the National Academy of Sciences of the United States of America, 106(45), 19179-19184, 2009). However, because these studies do not separate the effect of reward from the effect of practice, it is difficult to determine whether the effect of reward on learning is distinct from the effect of corrective feedback on learning. Thus, it is unknown whether these group differences in learning are due to reward processing or learning in general. Here, we compared the performance of medicated PD patients to demographically matched healthy controls (HCs) on a task where the effect of reward can be examined separately from the effect of practice. We found that patients with PD showed significantly less reward-related learning improvements compared to HCs. In addition, stronger learning of rewarded associations over unrewarded associations was significantly correlated with smaller skin-conductance responses for HCs but not PD patients. These results demonstrate that when separating the effect of reward from the effect of corrective feedback, PD patients do not benefit from reward.
Subject(s)
Brain/physiology , Feedback, Psychological/physiology , Learning/physiology , Parkinson Disease/physiopathology , Reward , Adult , Female , Humans , Male , Neuropsychological Tests , Parkinson Disease/complications , Photic Stimulation/methods , Young AdultABSTRACT
Categorical learning is dependent on feedback. Here, we compare how positive and negative feedback affect information-integration (II) category learning. Ashby and O'Brien (2007) demonstrated that both positive and negative feedback are required to solve II category problems when feedback was not guaranteed on each trial, and reported no differences between positive-only and negative-only feedback in terms of their effectiveness. We followed up on these findings and conducted 3 experiments in which participants completed 2,400 II categorization trials across three days under 1 of 3 conditions: positive feedback only (PFB), negative feedback only (NFB), or both types of feedback (CP; control partial). An adaptive algorithm controlled the amount of feedback given to each group so that feedback was nearly equated. Using different feedback control procedures, Experiments 1 and 2 demonstrated that participants in the NFB and CP group were able to engage II learning strategies, whereas the PFB group was not. Additionally, the NFB group was able to achieve significantly higher accuracy than the PFB group by Day 3. Experiment 3 revealed that these differences remained even when we equated the information received on feedback trials. Thus, negative feedback appears significantly more effective for learning II category structures. This suggests that the human implicit learning system may be capable of learning in the absence of positive feedback.
Subject(s)
Concept Formation/physiology , Feedback, Psychological/physiology , Learning/physiology , Adult , Humans , Young AdultABSTRACT
Motor cortical (M1) transcranial magnetic stimulation (TMS) increases corticospinal output and improves motor learning when delivered during sensorimotor mu rhythm trough but not peak phases, suggesting that mechanisms supporting motor learning may be most active during mu trough phases. If so, learning-related corticospinal plasticity should be most evident during mu trough phases. Healthy adults were assigned to either a sequence or control group. Participants in the sequence group practiced the implicit serial reaction time task (SRTT), which contained an embedded, repeating 12-item sequence. Participants in the control group practiced a version of the SRTT that contained no sequence. We measured mu phase-independent and phase-dependent MEP amplitudes using EEG-informed single-pulse TMS before, immediately, and 30 minutes after the SRTT in both groups. All participants performed a retention test one hour after SRTT acquisition. In both groups, mu phase-independent MEP amplitudes increased following SRTT acquisition, but the pattern of mu phase-dependent MEP amplitude increases after SRTT acquisition differed between groups. MEP amplitude changes from baseline to 30 minutes after SRTT acquisition more strongly differed across phases in the control relative to the sequence group, with the control group showing smaller increases in peak- than trough-specific MEPs. Contrary to our original hypothesis, results revealed that sequence learning recruits peak- rather than trough-specific neurophysiological mechanisms. Overall, these findings suggest that mu peak phases may provide protected time windows for motor memory consolidation and demonstrate the presence of a mu phase-dependent motor learning mechanism in the human brain. Significance statement: Recent work suggests that the neurophysiological mechanisms supporting motor learning may be most active during sensorimotor mu rhythm trough phases. Here, we evaluated this possibility by measuring mu phase-dependent corticospinal plasticity induced by motor sequence learning. Results provide first evidence that motor sequence learning produced corticospinal plasticity that was more pronounced during mu peak than trough phases, demonstrating the presence of a phase-dependent learning mechanism within the human motor system.
ABSTRACT
The hippocampal and caudate networks interact to support episodic memory, but the relationship between hippocampal and caudate connectivity strength and episodic memory is unclear. In general, cognition is optimally supported when connectivity within a functional network dominates connectivity from other networks. For example, episodic memory may be optimally supported when the hippocampal and caudate networks express this pattern of connectivity, consistent with research showing that the two networks are organized competitively. Alternatively, episodic memory may be optimally supported when connectivity in both networks is more balanced, consistent with fMRI reports showing cooperation between networks. Using cross-sectional behavioral and resting state fMRI data from a diverse sample (N = 347; Ages 18-85), I tested the hypothesis that reduced hippocampal and caudate network dominance would be associated with reduced episodic memory across individuals and age. Consistent with this hypothesis, lower caudate network dominance in bilateral thalamic regions was associated with worse episodic memory regardless of age. Age-related differences in caudate network dominance in the pallidum and putamen were also associated with worse episodic memory performance, but through their shared variance with age. I found no evidence that network dominance was related to processing speed or executive function, or that hippocampal network dominance was relate to episodic memory performance. These results show that ongoing biological dynamics between the hippocampal and caudate networks throughout adulthood are related to episodic memory performance and support a growing literature specifying the role of the caudate network in episodic memory.
Subject(s)
Memory, Episodic , Humans , Adult , Cross-Sectional Studies , Hippocampus/diagnostic imaging , Cognition , Magnetic Resonance ImagingABSTRACT
Prism adaptation (PA) is a form of visuomotor training that produces both sensorimotor and cognitive aftereffects depending on the direction of the visual displacement. Recently, a neural framework explaining both types of PA-induced aftereffects has been proposed, but direct evidence for it is lacking. We employed Structural Equation Modeling (SEM), a form of effective connectivity analysis, to establish directionality among connected nodes of the brain network thought to subserve PA. The findings reveal two distinct network branches: (1) a loop involving connections from the parietal cortices to the right parahippocampal gyrus, and (2) a branch linking the lateral premotor cortex to the parahippocampal gyrus via the cerebellum. Like the sensorimotor aftereffects, the first branch exhibited qualitatively different modulations for left versus right PA, and critically, changes in these connections were correlated with the magnitude of the sensorimotor aftereffects. Like the cognitive aftereffects, changes in the second branch were qualitatively similar for left and right PA, with greater change for left PA and a trend correlation with cognitive aftereffects. These results provide direct evidence that PA is supported by two functionally distinct subnetworks, a parietal-temporal network responsible for sensorimotor aftereffects and a fronto-cerebellar network responsible for cognitive aftereffects.
ABSTRACT
Repetitive transcranial magnetic stimulation (rTMS) targeted to the hippocampal network via the inferior parietal cortex (HN-Stim) can strengthen hippocampal-cortical connectivity and improve episodic memory, offering a potential clinical intervention. However, acceptance of this technique has been tempered by the infrequent reproduction of findings in rTMS research on cognitive processes. We tested the reproducibility of the HN-Stim effect on episodic memory in our laboratory using different procedures from those previously published. We tested episodic memory in 29 participants before, one day, and one week after, three consecutive days of 20 Hz HN-Stim. Participants received stimulation targeted to either the area of inferior parietal cortex maximally connected to the left anterior hippocampus (HN-Stim; N = 14) or the vertex (control; N = 15), where we expected no effect. HN-Stim increased episodic memory performance one day, but not one week, after the last stimulation session. While failing to reproduce the lasting beneficial effect on memory found by others after five days of treatment, we found robust effects on behavior 24 h after treatment. HN-Stim is a safe and reliable means of enhancing episodic memory and may have potential for boosting learning and treating memory deficits.
Subject(s)
Hippocampus/physiology , Memory, Episodic , Nerve Net/physiology , Transcranial Magnetic Stimulation , Adult , Humans , Parietal Lobe/physiology , Reproducibility of Results , Transcranial Magnetic Stimulation/standardsABSTRACT
The striatum and medial temporal lobes (MTL) exhibit dissociable roles during learning. Whereas the striatum and its network of thalamic relays and cortical nodes are necessary for nondeclarative learning, the MTL and associated network are required for declarative learning. Several studies have suggested that these networks are functionally competitive during learning. Since these discoveries, however, evidence has accumulated that they can operate in a cooperative fashion. In this review, we discuss evidence for both competition and cooperation between these systems during learning, with the aim of reconciling these seemingly contradictory findings. Examples of cooperation between the striatum and MTL have been provided, especially during consolidation and generalization of knowledge, and do not appear to be precluded by differences in functional specialization. However, whether these systems cooperate or compete does seem to depend on the phase of learning and cognitive or motor aspects of the task. The involvement of other regions, such as midbrain dopaminergic nuclei and the prefrontal cortex, may promote and mediate cooperation between the striatum and the MTL during learning. Building on this body of research, we propose a model for striatum-MTL interactions in learning and memory and attempt to predict, in general terms, when cooperation or competition will occur.
Subject(s)
Drosophila Proteins/physiology , Learning/physiology , Nerve Net/physiology , Temporal Lobe/physiology , HumansABSTRACT
The ability to interpret transcranial magnetic stimulation (TMS)-evoked electroencephalography (EEG) potentials (TEPs) is limited by artifacts, such as auditory evoked responses produced by discharge of the TMS coil. TEPs generated from direct cortical stimulation should vary in their topographical activity pattern according to stimulation site and differ from responses to sham stimulation. Responses that do not show these effects are likely to be artifactual. In 20 healthy volunteers, we delivered active and sham TMS to the right prefrontal, left primary motor, and left posterior parietal cortex and compared the waveform similarity of TEPs between stimulation sites and active and sham TMS using a cosine similarity-based analysis method. We identified epochs after the stimulus when the spatial pattern of TMS-evoked activation showed greater than random similarity between stimulation sites and sham vs. active TMS, indicating the presence of a dominant artifact. To do this, we binarized the derivatives of the TEPs recorded from 30 EEG channels and calculated cosine similarity between conditions at each time point with millisecond resolution. Only TEP components occurring before approximately 80 ms differed across stimulation sites and between active and sham, indicating site and condition-specific responses. We therefore conclude that, in the absence of noise masking or other measures to decrease neural artifact, TEP components before about 80 ms can be safely interpreted as stimulation location-specific responses to TMS, but components beyond this latency should be interpreted with caution due to high similarity in their topographical activity pattern.
Subject(s)
Evoked Potentials, Auditory/physiology , Motor Cortex/physiology , Parietal Lobe/physiology , Transcranial Magnetic Stimulation , Adult , Brain Mapping , Electroencephalography , Female , Healthy Volunteers , Humans , Male , Young AdultABSTRACT
Wang et al. (2014) found that that five daily sessions of repetitive transcranial magnetic stimulation (rTMS) of the posterior parietal cortex (PPC) significantly increased functional connectivity (FC) in a network centered on the hippocampus, and caused a correlated increase in memory performance. However, this finding has not been reproduced independently and the requirement for five sessions has not been validated. We aimed to reproduce the imaging results of this experiment, focusing on hippocampal FC changes and using fewer days of rTMS. We measured resting state FC before and after three (N = 9) or four (N = 6) consecutive daily PPC rTMS sessions, using similar delivery parameter settings as Wang et al. (2014) Eight subjects received 3 d of rTMS delivered to the vertex as a control. We employed whole-brain and hypothesis-based statistical approaches to test for hippocampal FC changes. Additionally, we calculated FC in 17 brain networks to determine whether the topographic pattern of FC change was similar between studies. We did not include behavioral testing in this study. PPC, but not vertex, rTMS caused significant changes in hippocampal FC to the same regions as in the previous study. Brain-wide changes in hippocampal FC significantly exceeded changes in global connectedness, indicating that the effect of PPC rTMS was specific to the hippocampal network. Baseline hippocampal FC, measured before receiving stimulation, predicted the degree of rTMS-induced hippocampal FC as in the previous study. These findings reproduce the imaging findings of Wang et al. (2014) and show that FC enhancement can occur after only three to four sessions of PPC rTMS.
Subject(s)
Hippocampus/physiology , Neural Pathways/physiology , Parietal Lobe/physiology , Transcranial Direct Current Stimulation/methods , Adult , Female , Humans , Male , Reproducibility of Results , Young AdultABSTRACT
Compared with young adults, older adults demonstrate difficulty forming and retrieving episodic memories. One proposed mechanism is that older adults are impaired at binding information into nonoverlapping representations, which is a key function of the hippocampus. The current experiments evaluate age differences in acquiring new memories using a novel episodic associative learning (EAL) task designed to tap hippocampal-dependent binding. The task involved repeated exposure of stimuli pairs and required the formation of new representations of each stimulus pair, as each pair was mapped to a unique keypress response. Notably, individual stimuli appeared in multiple pairs, so pair retrieval was necessary for correct response production. Experiment 1 demonstrated that older adults learned more slowly, and less overall, than young adults on this task. We also found that older adults benefited less than young adults from correct responses and as the number of intervening pairs between repetitions of a pair increased, older adults showed larger decrements in accuracy than young adults. Experiment 2 replicated these findings while minimizing motor demands and providing more practice. We also measured processing speed and spatial reconstruction to determine the involvement of specific cognitive mechanisms in observed age effects. We found that young adults with better spatial reconstruction abilities performed better on the EAL task than young adults with lower abilities and older adults overall. These findings suggest that older adults' lower performance on the task may be partly explained by a decline in hippocampal-supported binding processes and a greater reliance on extrahippocampal learning systems. (PsycINFO Database Record
Subject(s)
Learning/physiology , Memory, Episodic , Adult , Age Factors , Female , Humans , Male , Middle Aged , Young AdultABSTRACT
Visuospatial cognition has an inherent lateralized bias. Individual differences in the direction and magnitude of this bias are associated with asymmetrical D2/3 dopamine binding and dopamine system genotypes. Dopamine level affects feedback-based learning and dopamine signaling asymmetry is related to differential learning from reward and punishment. High D2 binding in the left hemisphere is associated with preference for reward. Prism adaptation (PA) is a simple sensorimotor technique, which modulates visuospatial bias according to the direction of the deviation. Left-deviating prism adaptation (LPA) induces rightward bias in healthy subjects. It is therefore possible that the right side of space increases in saliency along with left hemisphere dopaminergic activity. Right-deviating prism adaptation (RPA) has been used mainly as a control condition because it does not modulate behavior in healthy individuals. Since LPA induces a rightward visuospatial bias as a result of left hemisphere modulation, and higher dopaminergic activity in the left hemisphere is associated with preference for rewarding events we hypothesized that LPA would increase the preference for learning with reward. Healthy volunteers performed a computer-based probabilistic classification task before and after LPA or RPA. Consistent with our predictions, PA altered the preference for rewarded versus punished learning, with the LPA group exhibiting increased learning from reward. These results suggest that PA modulates dopaminergic activity in a lateralized fashion.
Subject(s)
Adaptation, Physiological/physiology , Feedback, Psychological/physiology , Functional Laterality/physiology , Learning/physiology , Reward , Visual Perception/physiology , Cognition/physiology , Female , Humans , Male , Photic Stimulation , Young AdultABSTRACT
Evidence from tasks that primarily tap either hippocampal- or striatal-based memory systems suggests that although these systems often compete for control of behavior, aging is associated with greater cooperation between them. This may stem from altered prefrontal cortex function. Here, we use a configural response task designed to engage both memory systems to test how age affects their interaction with cortical regions including the prefrontal cortex. We found that although older and younger adults learned just as well, older adults showed greater initial activation in cortical networks associated with visuospatial-action mapping and resolving conflict for competing memory representations. Older adults also showed greater functional coupling of the striatum with the left inferior frontal gyrus, in parallel with similar hippocampal coupling to ventral visual regions as young adults. Overall, our results support the proposal that aging is associated with more cooperative memory systems, but we did not find that greater cooperation is associated with less interaction between the prefrontal cortex and core memory system structures during learning.
Subject(s)
Cerebral Cortex/physiology , Cognitive Aging/physiology , Cognitive Aging/psychology , Healthy Aging/physiology , Healthy Aging/psychology , Learning/physiology , Memory/physiology , Cerebral Cortex/diagnostic imaging , Corpus Striatum/diagnostic imaging , Corpus Striatum/physiology , Hippocampus/diagnostic imaging , Hippocampus/physiology , Magnetic Resonance Imaging , Neuronal Plasticity , Prefrontal Cortex/diagnostic imaging , Prefrontal Cortex/physiologyABSTRACT
Reward has been shown to change behavior as a result of incentive learning (by motivating the individual to increase their effort) and instrumental learning (by increasing the frequency of a particular behavior). However, Palminteri et al. (2011) demonstrated that reward can also improve the incidental learning of a motor skill even when participants are unaware of the relationship between the reward and the motor act. Nonetheless, it remains unknown whether these effects of reward are the indirect results of manipulations of top-down factors. To identify the locus of the benefit associated with rewarded incidental learning, we used a chord-learning task (Seibel, 1963) in which the correct performance of some chords was consistently rewarded with points necessary to complete the block whereas the correct performance of other chords was not rewarded. Following training, participants performed a transfer phase without reward and then answered a questionnaire to assess explicit awareness about the rewards. Experiment 1 revealed that rewarded chords were performed more quickly than unrewarded chords, and there was little awareness about the relationship between chords and reward. Experiment 2 obtained similar findings with simplified responses to show that the advantage for rewarded stimulus combinations reflected more efficient binding of stimulus-response (S-R) associations, rather than a response bias for rewarded associations or improved motor learning. These results indicate that rewards can be used to significantly improve the learning of S-R associations without directly manipulating top-down factors. (PsycINFO Database Record
Subject(s)
Learning/physiology , Motivation/physiology , Pattern Recognition, Visual/physiology , Reward , Adolescent , Adult , Feedback , Female , Functional Laterality , Humans , Knowledge , Male , Photic Stimulation , Reaction Time , Transfer, Psychology , Young AdultABSTRACT
Age is often associated with a decline in cognitive abilities that are important for maintaining functional independence, such as learning new skills. Many forms of motor learning appear to be relatively well preserved with age, while learning tasks that involve associative binding tend to be negatively affected. The current study aimed to determine whether age differences exist on a configural response learning task, which includes aspects of motor learning and associative binding. Young (M = 24 years) and older adults (M = 66.5 years) completed a modified version of a configural learning task. Given the requirement of associative binding in the configural relationships between responses, we predicted older adults would show significantly less learning than young adults. Older adults demonstrated lower performance (slower reaction time and lower accuracy). However, contrary to our prediction, older adults showed similar rates of learning as indexed by a configural learning score compared to young adults. These results suggest that the ability to acquire knowledge incidentally about configural response relationships is largely unaffected by cognitive aging. The configural response learning task provides insight into the task demands that constrain learning abilities in older adults.