Memory retrieval effects as a function of differences in phenomenal experience.

Conscious experience and perception are restricted to a single perspective. Although evidence to suggest differences in phenomenal experience can produce observable differences in behavior, it is not well understood how these differences might influence memory. We used fMRI to scan n = 49 participants while they encoded and performed a recognition memory test for faces and words. We calculated a cognitive bias score reflecting individual participants' propensity toward either Visual Imagery or Internal Verbalization based on their responses to the Internal Representations Questionnaire (IRQ). Neither visual imagery nor internal verbalization scores were significantly correlated with memory performance. In the fMRI data, there were typical patterns of activation differences between words and faces during both encoding and retrieval. There was no effect of internal representation bias on fMRI activation during encoding. At retrieval, however, a bias toward visualization was positively correlated with memory-related activation for both words and faces in inferior occipital gyri. Further, there was a crossover interaction in a network of brain regions such that visualization bias was associated with greater activation for words and verbalization bias was associated with greater activation for faces, consistent with increased effort for non-preferred stimulus retrieval. These findings suggest that individual differences in cognitive representations affect neural activation across different types of stimuli, potentially affecting memory retrieval performance.

These things take time: what is the role of the hippocampus in recognition memory over extended delays?

In a clever experimental design, Tallman, Clark, and Smith (this issue) tested the changes in fMRI activation and functional connectivity in the hippocampus and cortex as a function of memory age. They found that activation changed according to a power function (both increasing and decreasing) in several cortical regions but not within the hippocampus or medial temporal lobe (MTL). Further, functional connectivity increased with memory age between cortical regions but decreased for the hippocampus. Taken together, these results offer strong support for the standard consolidation model. However, they leave open the question of what role the hippocampus plays in recognition memory performance.

The contributions of eye gaze fixations and target-lure similarity to behavioral and fMRI indices of pattern separation and pattern completion.

Pattern separation and pattern completion are generally studied in humans using mnemonic discrimination tasks such as the Mnemonic Similarity Task (MST) where participants identify similar lures and repeated items from a series of images. Failures to correctly discriminate lures are thought to reflect a failure of pattern separation and a propensity toward pattern completion. Recent research has challenged this perspective, suggesting that poor encoding rather than pattern completion accounts for the occurrence of false alarm responses to similar lures. In two experiments, participants completed a continuous recognition task version of the MST while eye movement (Experiments 1 and 2) and fMRI data (Experiment 2) were collected. In Experiment 1, we replicated the result that fixation counts at study predicted accuracy on lure trials (consistent with poor encoding predicting mnemonic discrimination performance), but this effect was not observed in our fMRI task. In both experiments, we found that target-lure similarity was a strong predictor of accuracy on lure trials. Further, we found that fMRI activation changes in the hippocampus were significantly correlated with the number of fixations at study for correct but not incorrect mnemonic discrimination judgments when controlling for target-lure similarity. Our findings indicate that while eye movements during encoding predict subsequent hippocampal activation changes for correct mnemonic discriminations, the predictive power of eye movements for activation changes for incorrect mnemonic discrimination trials was modest at best.

Investigation of the relationship between visual feature binding in short- and long-term memory in healthy aging.

Binding visual features into coherent object representations is essential both in short- and long-term memory. However, the relationship between feature binding processes at different memory delays remains unexplored. Here, we addressed this question by using the Mnemonic Similarity Task and a delayed-estimation working memory task on a large sample of older adults. The results revealed that higher propensity to misbind object features in working memory is associated with lower lure discrimination performance in the mnemonic similarity task, suggesting that shared feature binding processes underlie the formation of coherent short- and long-term visual object memory representations.

Pattern separation beyond the hippocampus: A high-resolution whole-brain investigation of mnemonic discrimination in healthy adults.

Episodic memory depends on the computational process of pattern separation in order to establish distinct memory representations of similar episodes. Studies of pattern separation in humans rely on mnemonic discrimination tasks, which have been shown to tax hippocampal-dependent pattern separation. Although previous neuroimaging research has focused on hippocampal processing, little is known about how other brain regions, known to be involved in recognition memory performance, are involved in mnemonic discrimination tasks. Conversely, neuroimaging studies of pattern separation with whole-brain coverage lack spatial resolution to localize activation to hippocampal subfields. In this study, 48 healthy young adult participants underwent whole-brain high-resolution functional MRI (fMRI) scanning while completing a mnemonic discrimination task. A priori region-of-interest analyses revealed activation patterns consistent with pattern separation in distinct hippocampal subregions, particularly in the subiculum. Connectivity analyses revealed a network of cortical regions consistent with the memory retrieval network where fMRI activation was correlated with hippocampal activation. An exploratory whole-brain analysis revealed widespread activation differentially associated with performance of the mnemonic discrimination task. Taken together, these results suggest that a network of brain regions contribute to mnemonic discrimination performance, with the hippocampus and parahippocampal cortex as a hub in the network displaying clear signals consistent with pattern separation and regions such as the dorsal medial prefrontal cortex particularly important for successful lure discrimination.

Does inhibitory control training reduce weight and caloric intake in adults with overweight and obesity? A pre-registered, randomized controlled event-related potential (ERP) study.

A cognitive intervention that may reduce weight and caloric intake is inhibitory control training (ICT; having individuals repeatedly withhold dominant responses to unhealthy food images). We conducted a randomized controlled trial where 100 individuals with overweight or obesity were assigned to complete a generic (n = 48) or food-specific ICT (n = 52) training four times per week for four weeks. Weight and caloric intake were obtained at baseline, four-weeks, and 12-weeks. Participants also completed high-calorie and neutral go/no-go tasks while N2 event-related potential (ERP) data, a neural indicator of inhibitory control, was measured at all visits. Results from mixed model analyses indicate that neither weight, caloric intake, nor N2 ERP component amplitude towards high-calorie foods changed at post-testing or at the 12-week follow up. Regression analyses suggest that individuals with smaller N2 difference amplitudes to food may show greater weight loss and reductions in caloric intake after a generic ICT, while individuals with larger N2 difference amplitudes to food may show greater weight loss and reductions in caloric intake after a food-specific ICT. Overall, multiple food-specific or generic ICT sessions over the course of a four-week period do not affect overall weight loss, caloric intake, or N2 ERP amplitude.

Acute after-school screen time in children decreases impulse control and activation toward high-calorie food stimuli in brain regions related to reward and attention.

The purpose of this study was to examine the effects of after-school sedentary screen time on children's brain activation in reward and cognitive control regions in response to pictures of high- and low-calorie foods. Thirty-two children participated in a randomized crossover study with counterbalanced treatment conditions. Conditions took place on separate days after school and included three hours of active or sedentary play. After each condition, neural activation was assessed using functional magnetic resonance imaging (fMRI) while participants completed a go/no-go task involving pictures of high- and low-calorie foods. General response inhibition was also measured using the Stroop task. Hunger was measured upon arrival to the testing facility and just prior to fMRI scans. Mixed effects models were used to evaluate main effects and interactions. Significant stimulus by condition interactions were found in the right superior parietal cortex, and left anterior cingulate cortex (Ps ≤ 0.05). High-calorie pictures elicited significantly more activation bilaterally in the orbitofrontal cortex compared to low-calorie pictures (Ps ≤ 0.05). Stroop task performance diminished significantly following the sedentary condition compared to the active (P ≤ 0.05). Subjective feelings of hunger were not different between conditions at any point. Sedentary screen time was associated with significantly decreased response inhibition and a reversed brain activation pattern to pictures of high- and low-calorie foods compared to active play, in areas of the brain important to the modulation of food intake. Decreased attention, and impulse control following sedentary screen time may contribute to disinhibited eating that can lead to overweight and obesity.

Repetition of Computer Security Warnings Results in Differential Repetition Suppression Effects as Revealed With Functional MRI.

Computer users are often the last line of defense in computer security. However, with repeated exposures to system messages and computer security warnings, neural and behavioral responses show evidence of habituation. Habituation has been demonstrated at a neural level as repetition suppression where responses are attenuated with subsequent repetitions. In the brain, repetition suppression to visual stimuli has been demonstrated in multiple cortical areas, including the occipital lobe and medial temporal lobe. Prior research into the repetition suppression effect has generally focused on a single repetition and has not examined the pattern of signal suppression with repeated exposures. We used complex, everyday stimuli, in the form of images of computer programs or security warning messages, to examine the repetition suppression effect across repeated exposures. The use of computer warnings as stimuli also allowed us to examine the activation of learned fearful stimuli. We observed widespread linear decreases in activation with repeated exposures, suggesting that repetition suppression continues after the first repetition. Further, we found greater activation for warning messages compared to neutral images in the anterior insula, pre-supplemental motor area, and inferior frontal gyrus, suggesting differential processing of security warning messages. However, the repetition suppression effect was similar in these regions for both warning messages and neutral images. Additionally, we observed an increase of activation in the default mode network with repeated exposures, suggestive of increased mind wandering with continuing habituation.

White matter integrity disparities between normal-weight and overweight/obese adolescents: an automated fiber quantification tractography study.

Obese adults have been shown to have poorer white brain matter integrity relative to normal-weight peers, but few studies have tested whether white matter integrity is compromised in overweight and obese adolescents. Also, it is unclear if age interacts with body mass to affect white matter integrity in adolescents. We used Automated Fiber Quantification, a tractography method, to compare fractional anisotropy between normal-weight and overweight/obese adolescents in the corpus callosum, corticospinal tract, cingulum, inferior fronto-occipital fasciculus, and uncinate fasciculus. Further, we tested whether any differences were moderated by age. Forty-seven normal-weight and forty overweight/obese adolescents were scanned using a diffusion tensor imaging (DTI) scan sequence. Overweight/obese compared to normal-weight adolescents had decreased white matter integrity in the superior frontal corpus callosum, left and right uncinate fasciculi, left inferior fronto-occipital fasciculus, and left corticospinal tract, which may be related to heightened reward processing. Overweight/obese compared to normal-weight adolescents had increased white matter integrity in the orbital and anterior frontal corpus callosum, right inferior fronto-occipital fasciculus, left cingulum, and left corticospinal tract, which may be related to heightened attentional processing. As age increased, six tracts showed poorer white matter integrity as body mass index percentile (BMI%) increased, but three tracts showed greater white matter integrity as BMI% increased. Future research examining associations between white matter integrity and neural indices of food-related reward and attention are needed to clarify the functional significance of white matter integrity discrepancies between normal-weight and overweight/obese adolescents.

Mnemonic Similarity Task: A Tool for Assessing Hippocampal Integrity.

The hippocampus is critical for learning and memory, relying in part on pattern separation processes supported by the dentate gyrus (DG) to prevent interference from overlapping memory representations. In 2007, we designed the Mnemonic Similarity Task (MST), a modified object recognition memory task, to be highly sensitive to hippocampal function by placing strong demands on pattern separation. The MST is now a widely used behavioral task, repeatedly shown to be sensitive to age-related memory decline, hippocampal connectivity, and hippocampal function, with specificity to the DG. Here, we review the utility of the MST, its relationship to hippocampal function, its utility in detecting hippocampal-based memory alterations across the lifespan, and impairments associated with clinical pathology from a variety of disorders.

Efficacy of weight loss intervention can be predicted based on early alterations of fMRI food cue reactivity in the striatum.

Increased fMRI food cue reactivity in obesity, i.e. higher responses to high- vs. low-calorie food images, is a promising marker of the dysregulated brain reward system underlying enhanced susceptibility to obesogenic environmental cues. Recently, it has also been shown that weight loss interventions might affect fMRI food cue reactivity and that there is a close association between the alteration of cue reactivity and the outcome of the intervention. Here we tested whether fMRI food cue reactivity could be used as a marker of diet-induced early changes of neural processing in the striatum that are predictive of the outcome of the weight loss intervention. To this end we investigated the relationship between food cue reactivity in the striatum measured one month after the onset of the weight loss program and weight changes obtained at the end of the six-month intervention. We observed a significant correlation between BMI change measured after six months and early alterations of fMRI food cue reactivity in the striatum, including the bilateral putamen, right pallidum, and left caudate. Our findings provide evidence for diet-induced early alterations of fMRI food cue reactivity in the striatum that can predict the outcome of the weight loss intervention.

Sleep duration differentially affects brain activation in response to food images in adolescents with overweight/obesity compared to adolescents with normal weight.

STUDY OBJECTIVES: Sleep is an important behavior that affects appetite and eating in adolescents. Our study examined food-related neural activation in brain regions associated with food reward and inhibition in adolescents under sleep-restricted and well-rested conditions. METHODS: In this within-subjects study, 52 adolescents (ages 12-18; 46% female; M age = 15.96 years, SD = 1.56) with normal weight (NW; N = 29, M body mass index % [BMI%] = 54.55, SD = 24.54) or overweight/obesity (OV/OB; N = 23, M BMI% = 93.78, SD = 4.60) spent 5 hours in bed at home each night for five consecutive nights and 9 hours in bed at home each night for 5 consecutive nights, with the first day of each condition occurring 4 weeks apart. The morning following each sleep modification period, functional magnetic resonance imaging (fMRI) data were collected while participants performed an inhibitory (go/no-go) task with food stimuli. RESULTS: We found significantly greater activation in brain regions associated with inhibition in adolescents with NW in response to food cues when sleep restricted. No increase in inhibition-related neural activation was observed in adolescents with OV/OB when sleep restricted. We also found neural activation consistent with greater reward processing associated with food cues following sleep restriction regardless of weight status. CONCLUSIONS: These findings suggest that chronic sleep restriction may increase the likelihood of suboptimal dietary behavior for adolescents with OV/OB because they do not experience increased inhibition-related neural responding to counter possible increased reward-related neural responding following sleep restriction.

Brain reactivity to visual food stimuli after moderate-intensity exercise in children.

Exercise may play a role in moderating eating behaviors. The purpose of this study was to examine the effect of an acute bout of exercise on neural responses to visual food stimuli in children ages 8-11 years. We hypothesized that acute exercise would result in reduced activity in reward areas of the brain. Using a randomized cross-over design, 26 healthy weight children completed two separate laboratory conditions (exercise; sedentary). During the exercise condition, each participant completed a 30-min bout of exercise at moderate-intensity (~ 67% HR maximum) on a motor-driven treadmill. During the sedentary session, participants sat continuously for 30 min. Neural responses to high- and low-calorie pictures of food were determined immediately following each condition using functional magnetic resonance imaging. There was a significant exercise condition*stimulus-type (high- vs. low-calorie pictures) interaction in the left hippocampus and right medial temporal lobe (p < 0.05). Main effects of exercise condition were observed in the left posterior central gyrus (reduced activation after exercise) (p < 0.05) and the right anterior insula (greater activation after exercise) (p < 0.05). The left hippocampus, right medial temporal lobe, left posterior central gyrus, and right anterior insula appear to be activated by visual food stimuli differently following an acute bout of exercise compared to a non-exercise sedentary session in 8-11 year-old children. Specifically, an acute bout of exercise results in greater activation to high-calorie and reduced activation to low-calorie pictures of food in both the left hippocampus and right medial temporal lobe. This study shows that response to external food cues can be altered by exercise and understanding this mechanism will inform the development of future interventions aimed at altering energy intake in children.

The effects of sleep on the neural correlates of pattern separation.

Effective memory representations must be specific to prevent interference between episodes that may overlap in terms of place, time, or items present. Pattern separation, a computational process performed by the hippocampus, overcomes this interference by establishing nonoverlapping memory representations. Although it is widely accepted that declarative memories are consolidated during sleep, the effects of sleep on pattern separation have yet to be elucidated. We used whole-brain, high-resolution functional neuroimaging to investigate the effects of sleep on a task that places high demands on pattern separation. Sleep had a selective effect on memory specificity and not general recognition memory. Activity in brain regions related to memory retrieval and cognitive control demonstrated an interaction between sleep and delay. Surprisingly, there was no effect of sleep on hippocampal activity using a group-level analysis. To further understand the role of the hippocampus on our task, we performed a representational similarity analysis, which showed that hippocampal activation was biased toward pattern separation relative to cortical activation and that this bias increased following a delay (regardless of sleep). Cortical activation, conversely, was biased toward pattern completion and this bias was preferentially enhanced by sleep.

A direct comparison between ERP and fMRI measurements of food-related inhibitory control: Implications for BMI status and dietary intake.

Obesity and maintaining a healthy diet have important implications for physical and mental health. One factor that may influence diet and obesity is inhibitory control. We tested how N2 and P3 amplitude, event-related potential (ERP) components that reflect inhibitory control, and functional magnetic resonance imaging (fMRI) activity in brain regions associated with inhibitory control differed toward high- and low-calorie food stimuli across BMI status. We also assessed the relationship between neural indices of food-related inhibitory control and laboratory and daily food intake. Fifty-four individuals (17 normal-weight; 18 overweight; 19 individuals with obesity) completed two food-based go/no-go tasks (one with high- and one with low-calorie foods as no-go stimuli), once during ERP data acquisition and once during fMRI data acquisition. After testing, participants were presented with an ad libitum weighed food buffet. Participants also recorded their food intake using the Automated Self-Administered 24-hour Dietary Recall (ASA24) system across four days. Individuals recruited more inhibitory control when withholding responses towards high-compared to low-calorie foods, although this effect was more consistent for N2 than P3 or fMRI assessments. BMI status did not influence food-related inhibitory control. A larger inhibitory response as measured by N2 amplitude was related to increased ASA24 food intake; P3 amplitude and fMRI region of interest activity did not predict ASA24 intake; neither method predicted food intake from the buffet. ERP and fMRI measurements show similar neural responses to food, although N2 amplitude may be somewhat more sensitive in detecting differences between food types and predicting self-reports of food intake.

Discrete pre-processing step effects in registration-based pipelines, a preliminary volumetric study on T1-weighted images.

Pre-processing MRI scans prior to performing volumetric analyses is common practice in MRI studies. As pre-processing steps adjust the voxel intensities, the space in which the scan exists, and the amount of data in the scan, it is possible that the steps have an effect on the volumetric output. To date, studies have compared between and not within pipelines, and so the impact of each step is unknown. This study aims to quantify the effects of pre-processing steps on volumetric measures in T1-weighted scans within a single pipeline. It was our hypothesis that pre-processing steps would significantly impact ROI volume estimations. One hundred fifteen participants from the OASIS dataset were used, where each participant contributed three scans. All scans were then pre-processed using a step-wise pipeline. Bilateral hippocampus, putamen, and middle temporal gyrus volume estimations were assessed following each successive step, and all data were processed by the same pipeline 5 times. Repeated-measures analyses tested for a main effects of pipeline step, scan-rescan (for MRI scanner consistency) and repeated pipeline runs (for algorithmic consistency). A main effect of pipeline step was detected, and interestingly an interaction between pipeline step and ROI exists. No effect for either scan-rescan or repeated pipeline run was detected. We then supply a correction for noise in the data resulting from pre-processing.

Long-term cognitive and neuroanatomical stability in patients with anoxic amnesia: A Case Report.

BACKGROUND: Anoxia can result in selective hippocampal damage with associated impairments in declarative memory. Whilst memory impairments and brain structures are thought to be stable, there are little data regarding the effects of ageing or change over time in patients with amnesia from anoxic brain injury. METHODS: To assess change over time, we compared structural magnetic resonance imaging (MRI) with data obtained over ten years previously in two well-characterized patients with amnesia (JRW and RS) who experienced an anoxic brain injury. Six healthy, age-matched control participants were recruited to compare brain volumes with the patients at Time 2. Wechsler adult intelligence scale-revised and Wechsler memory scale-revised scores were compared to scores on the same tests administered 13 and 19 years prior. RESULTS: Patients with amnesia had significantly smaller hippocampal volumes than controls, but comparable medial temporal lobe and ventricular volumes. Memory, intellectual function and brain volumes were stable over time. CONCLUSION: Patients with an amnesia due to anoxia have memory impairments and smaller hippocampal volumes compared to controls; however, memory, intelligence and structural volumes remain stable over time. At ages 50 and 57, they do not appear to have early age-associated cognitive decline that is sometimes observed in patients with traumatic brain injury.

An event-related potential investigation of pattern separation and pattern completion processes.

Long-term declarative memory depends on pattern separation and pattern completion to maintain memory specificity. Previous studies aimed at evaluating the underlying neuronal substrates of these computational processes have used a mnemonic discrimination paradigm and functional magnetic resonance imaging (fMRI). An alternative method is electroencephalography and event-related potentials (ERPs), which have a superior time resolution to fMRI. Here, we use ERP analysis to examine neuronal activity during performance of a mnemonic discrimination task. We examined both the late positive component and FN400 components, which have previously been shown to demonstrate an old-new effect. We hypothesized that pattern separation processes would be reflected in correct rejection of similar lures while pattern completion processes would be reflected in falsely categorizing lures as repeated. We did not observe differences between the ERPs associated with these two processes.

Motivational Impact of Palatable Food Correlates With Functional Brain Responses to Food Images in Adolescents.

Objective: To examine associations between motivational impact of palatable foods and neural activity in brain regions involved in inhibitory control among adolescents. Methods: Thirty-four adolescents aged 14-20 years underwent functional magnetic resonance imaging while viewing images of high- and low-energy foods. Participants completed the Power of Food Scale (PFS). Whole-brain analyses of variance tested for neural activation differences and correlations between brain activation and PFS scores were tested. Results: We found an interaction between food type (high energy vs. low energy) and PFS scores in the right dorsolateral prefrontal cortex and right inferior parietal lobule. We also found that PFS scores correlated negatively with activation to high-energy foods in prefrontal cortical and parietal regions. Conclusions: These findings suggest that individuals with high motivation for high-energy foods also demonstrate lower neural activation in inhibition-related brain regions when viewing images of high-energy foods, indicating that they may have difficulty inhibiting consumption impulses.

Event-related potential indices of congruency sequence effects without feature integration or contingency learning confounds.

The congruency effect in Stroop-like tasks (i.e., increased response time and reduced accuracy in incongruent relative to congruent trials) is often smaller when the previous trial was incongruent as compared to congruent. This congruency sequence effect (CSE) is thought to reflect cognitive control processes that shift attention to the target and/or modulate the response engendered by the distracter differently after incongruent relative to congruent trials. The neural signatures of CSEs are therefore usually attributed to cognitive control processes that minimize distraction from irrelevant stimuli. However, CSEs in previous functional neuroimaging studies were ubiquitously confounded with feature integration and/or contingency learning processes. We therefore investigated whether a neural CSE can be observed without such confounds in a group of healthy young adults (n = 56). To this end, we combined a prime-probe task that lacks such confounds with high-density ERPs to identify, for the first time, the neural time course of confound-minimized CSEs. Replicating recent behavioral findings, we observed strong CSEs in this task for mean response time and mean accuracy. Critically, conceptually replicating prior ERP results from confounded tasks, we also observed a CSE in both the parietal conflict slow potential (conflict SP) and the frontomedial N450. These findings indicate for the first time that neural CSEs as indexed by ERPs can be observed without the typical confounds. More broadly, the present study provides a confound-minimized protocol that will help future researchers to better isolate the neural bases of control processes that minimize distraction from irrelevant stimuli.