Characterizing the role of impulsivity in costly, reactive aggression using a novel paradigm.

A lack of self-control has long been theorized to predict an individual's likelihood to engage in antisocial behaviors. However, existing definitions of self-control encompass multiple psychological constructs and lab-based measures of aggression have not allowed for the examination of aggression upon provocation where self-control is needed most. We introduce two versions of a novel paradigm, the Retaliate or Carry-on: Reactive AGgression Experiment (RC-RAGE) to fill this methodological gap. Using large online samples of US adults (N = 354 and N = 366), we evaluate to what extent dispositional impulsivity, self-control, aggression, and state anger contribute to aggression upon provocation when there is a financial cost involved. Results showed that costly retaliation on this task was related to trait aggression and being in an angry emotional state, but not related to social desirability. Importantly, we show that the tendency to act impulsively is a better predictor of costly retaliation than other forms of self-control, such as the ability to delay gratification, resist temptation, or plan ahead. As a browser-based task, the RC-RAGE provides a tool for the future investigation of reactive aggression in a variety of experimental settings.

Visuospatial information foraging describes search behavior in learning latent environmental features.

In the real world, making sequences of decisions to achieve goals often depends upon the ability to learn aspects of the environment that are not directly perceptible. Learning these so-called latent features requires seeking information about them. Prior efforts to study latent feature learning often used single decisions, used few features, and failed to distinguish between reward-seeking and information-seeking. To overcome this, we designed a task in which humans and monkeys made a series of choices to search for shapes hidden on a grid. On our task, the effects of reward and information outcomes from uncovering parts of shapes could be disentangled. Members of both species adeptly learned the shapes and preferred to select tiles expected to be informative earlier in trials than previously rewarding ones, searching a part of the grid until their outcomes dropped below the average information outcome-a pattern consistent with foraging behavior. In addition, how quickly humans learned the shapes was predicted by how well their choice sequences matched the foraging pattern, revealing an unexpected connection between foraging and learning. This adaptive search for information may underlie the ability in humans and monkeys to learn latent features to support goal-directed behavior in the long run.

Item memorability has no influence on value-based decisions.

While making decisions, we often rely on past experiences to guide our choices. However, not all experiences are remembered equally well, and some elements of an experience are more memorable than others. Thus, the intrinsic memorability of past experiences may bias our decisions. Here, we hypothesized that individuals would tend to choose more memorable options than less memorable ones. We investigated the effect of item memorability on choice in two experiments. First, using food images, we found that the same items were consistently remembered, and others consistently forgotten, across participants. However, contrary to our hypothesis, we found that participants did not prefer or choose the more memorable over the less memorable items when choice options were matched for the individuals' valuation of the items. Second, we replicated these findings in an alternate stimulus domain, using words that described the same food items. These findings suggest that stimulus memorability does not play a significant role in determining choice based on subjective value.

Neural Representations of Food-Related Attributes in the Human Orbitofrontal Cortex during Choice Deliberation in Anorexia Nervosa.

Decisions about what to eat recruit the orbitofrontal cortex (OFC) and involve the evaluation of food-related attributes such as taste and health. These attributes are used differently by healthy individuals and patients with disordered eating behavior, but it is unclear whether these attributes are decodable from activity in the OFC in both groups and whether neural representations of these attributes are differentially related to decisions about food. We used fMRI combined with behavioral tasks to investigate the representation of taste and health attributes in the human OFC and the role of these representations in food choices in healthy women and women with anorexia nervosa (AN). We found that subjective ratings of tastiness and healthiness could be decoded from patterns of activity in the OFC in both groups. However, health-related patterns of activity in the OFC were more related to the magnitude of choice preferences among patients with AN than healthy individuals. These findings suggest that maladaptive decision-making in AN is associated with more consideration of health information represented by the OFC during deliberation about what to eat.SIGNIFICANCE STATEMENT An open question about the OFC is whether it supports the evaluation of food-related attributes during deliberation about what to eat. We found that healthiness and tastiness information was decodable from patterns of neural activity in the OFC in both patients with AN and healthy controls. Critically, neural representations of health were more strongly related to choices in patients with AN, suggesting that maladaptive overconsideration of healthiness during deliberation about what to eat is related to activity in the OFC. More broadly, these results show that activity in the human OFC is associated with the evaluation of relevant attributes during value-based decision-making. These findings may also guide future research into the development of treatments for AN.

Memory for individual items is related to nonreinforced preference change.

It is commonly assumed that memories contribute to value-based decisions. Nevertheless, most theories of value-based decision-making do not account for memory influences on choice. Recently, new interest has emerged in the interactions between these two fundamental processes, mainly using reinforcement-based paradigms. Here, we aimed to study the role memory processes play in preference change following the nonreinforced cue-approach training (CAT) paradigm. In CAT, the mere association of cued items with a speeded motor response influences choices. Previous studies with this paradigm showed that a single training session induces a long-lasting effect of enhanced preferences for high-value trained stimuli, that is maintained for several months. We hypothesized that CAT increases memory of trained items, leading to enhanced accessibility of their positive associative memories and in turn to preference changes. In two preregistered experiments, we found evidence that memory is enhanced for trained items and that better memory is correlated with enhanced preferences at the individual item level, both immediately and 1 mo following CAT. Our findings suggest that memory plays a central role in value-based decision-making following CAT, even in the absence of external reinforcements. These findings contribute to new theories relating memory and value-based decision-making and set the groundwork for the implementation of novel nonreinforced behavioral interventions that lead to long-lasting behavioral change.

What Are Memories For? The Hippocampus Bridges Past Experience with Future Decisions.

Many decisions require flexible reasoning that depends on inference, generalization, and deliberation. Here, we review emerging findings indicating that the hippocampus, known for its role in long-term memory, contributes to these flexible aspects of value-based decision-making. This work offers new insights into the role of memory in decision-making and suggests that memory may shape decisions even in situations that do not appear, at first glance, to depend on memory at all. Uncovering the pervasive role of memory in decision-making challenges the way we define what memory is and what it does, suggesting that memory's primary purpose may be to guide future behavior and that storing a record of the past is just one way to do so.

Food Folio by Columbia Center for Eating Disorders: A Freely Available Food Image Database.

Food images are useful stimuli for the study of cognitive processes as well as eating behavior. To enhance rigor and reproducibility in task-based research, it is advantageous to have stimulus sets that are publicly available and well characterized. Food Folio by Columbia Center for Eating Disorders is a publicly available set of 138 images of Western food items. The set was developed for the study of eating disorders, particularly for use in tasks that capture eating behavior characteristic of these illnesses. It contains foods that are typically eaten, as well as those typically avoided, by individuals with eating disorders. Each image has now been rated across 17 different attributes by a large general United States population sample via Amazon's Mechanical Turk (n = 1054). Ratings included subjective attributes (e.g., tastiness, healthiness, and favorable texture) as well as estimates of nutrient content (e.g., fat and carbohydrate). Each participant rated a subset of stimulus set food items (46 foods) on all 17 dimensions. Additional description of the image set is provided in terms of physical image information and accurate nutritional information. Correlations between subjective ratings were calculated and an exploratory factor analysis and exploratory cluster analysis completed. Outcomes of the factor analysis suggested foods may be described along three latent factors of healthiness, tastiness, and umami taste; the cluster analysis highlighted five distinct clusters of foods varying on these same dimensions. Descriptive outcomes indicated that the stimulus set includes a range of foods that vary along multiple dimensions and thus is likely to be useful in addressing various research questions surrounding eating behavior and cognition in healthy populations, as well as in those with eating disorders. The provision of comprehensive descriptive information allows for stimulus selection that is optimized for a given research question and promotes strong inference.

The hippocampus supports deliberation during value-based decisions.

Choosing between two items involves deliberation and comparison of the features of each item and its value. Such decisions take more time when choosing between options of similar value, possibly because these decisions require more evidence, but the mechanisms involved are not clear. We propose that the hippocampus supports deliberation about value, given its well-known role in prospection and relational cognition. We assessed the role of the hippocampus in deliberation in two experiments. First, using fMRI in healthy participants, we found that BOLD activity in the hippocampus increased as a function of deliberation time. Second, we found that patients with hippocampal damage exhibited more stochastic choices and longer reaction times than controls, possibly due to their failure to construct value-based or internal evidence during deliberation. Both sets of results were stronger in value-based decisions compared to perceptual decisions.

Spacing of cue-approach training leads to better maintenance of behavioral change.

The maintenance of behavioral change over the long term is essential to achieve public health goals such as combatting obesity and drug use. Previous work by our group has demonstrated a reliable shift in preferences for appetitive foods following a novel non-reinforced training paradigm. In the current studies, we tested whether distributing training trials over two consecutive days would affect preferences immediately after training as well as over time at a one-month follow-up. In four studies, three different designs and an additional pre-registered replication of one sample, we found that spacing of cue-approach training induced a shift in food choice preferences over one month. The spacing and massing schedule employed governed the long-term changes in choice behavior. Applying spacing strategies to training paradigms that target automatic processes could prove a useful tool for the long-term maintenance of health improvement goals with the development of real-world behavioral change paradigms that incorporate distributed practice principles.

Neural mechanisms of cue-approach training.

Biasing choices may prove a useful way to implement behavior change. Previous work has shown that a simple training task (the cue-approach task), which does not rely on external reinforcement, can robustly influence choice behavior by biasing choice toward items that were targeted during training. In the current study, we replicate previous behavioral findings and explore the neural mechanisms underlying the shift in preferences following cue-approach training. Given recent successes in the development and application of machine learning techniques to task-based fMRI data, which have advanced understanding of the neural substrates of cognition, we sought to leverage the power of these techniques to better understand neural changes during cue-approach training that subsequently led to a shift in choice behavior. Contrary to our expectations, we found that machine learning techniques applied to fMRI data during non-reinforced training were unsuccessful in elucidating the neural mechanism underlying the behavioral effect. However, univariate analyses during training revealed that the relationship between BOLD and choices for Go items increases as training progresses compared to choices of NoGo items primarily in lateral prefrontal cortical areas. This new imaging finding suggests that preferences are shifted via differential engagement of task control networks that interact with value networks during cue-approach training.

Mechanisms of Choice Behavior Shift Using Cue-approach Training.

Cue-approach training has been shown to effectively shift choices for snack food items by associating a cued button-press motor response to particular food items. Furthermore, attention was biased toward previously cued items, even when the cued item is not chosen for real consumption during a choice phase. However, the exact mechanism by which preferences shift during cue-approach training is not entirely clear. In three experiments, we shed light on the possible underlying mechanisms at play during this novel paradigm: (1) Uncued, wholly predictable motor responses paired with particular food items were not sufficient to elicit a preference shift; (2) Cueing motor responses early - concurrently with food item onset - and thus eliminating the need for heightened top-down attention to the food stimulus in preparation for a motor response also eliminated the shift in food preferences. This finding reinforces our hypothesis that heightened attention at behaviorally relevant points in time is key to changing choice behavior in the cue-approach task; (3) Crucially, indicating choice using eye movements rather than manual button presses preserves the effect, thus demonstrating that the shift in preferences is not governed by a learned motor response but more likely via modulation of subjective value in higher associative regions, consistent with previous neuroimaging results. Cue-approach training drives attention at behaviorally relevant points in time to modulate the subjective value of individual items, providing a mechanism for behavior change that does not rely on external reinforcement and that holds great promise for developing real world behavioral interventions.

Neural correlates of state-based decision-making in younger and older adults.

Older and younger adults performed a state-based decision-making task while undergoing functional MRI (fMRI). We proposed that younger adults would be more prone to base their decisions on expected value comparisons, but that older adults would be more reactive decision-makers who would act in response to recent changes in rewards or states, rather than on a comparison of expected values. To test this we regressed BOLD activation on two measures from a sophisticated reinforcement learning (RL) model. A value-based regressor was computed by subtracting the immediate value of the selected alternative from its long-term value. The other regressor was a state-change uncertainty signal that served as a proxy for whether the participant's state improved or declined, relative to the previous trial. Younger adults' activation was modulated by the value-based regressor in ventral striatal and medial PFC regions implicated in reinforcement learning. Older adults' activation was modulated by state-change uncertainty signals in right dorsolateral PFC, and activation in this region was associated with improved performance in the task. This suggests that older adults may depart from standard expected-value based strategies and recruit lateral PFC regions to engage in reactive decision-making strategies.

Changing value through cued approach: an automatic mechanism of behavior change.

It is believed that choice behavior reveals the underlying value of goods. The subjective values of stimuli can be changed through reward-based learning mechanisms as well as by modifying the description of the decision problem, but it has yet to be shown that preferences can be manipulated by perturbing intrinsic values of individual items. Here we show that the value of food items can be modulated by the concurrent presentation of an irrelevant auditory cue to which subjects must make a simple motor response (i.e., cue-approach training). Follow-up tests showed that the effects of this pairing on choice lasted at least 2 months after prolonged training. Eye-tracking during choice confirmed that cue-approach training increased attention to the cued items. Neuroimaging revealed the neural signature of a value change in the form of amplified preference-related activity in ventromedial prefrontal cortex.

Influencing food choices by training: evidence for modulation of frontoparietal control signals.

To overcome unhealthy behaviors, one must be able to make better choices. Changing food preferences is an important strategy in addressing the obesity epidemic and its accompanying public health risks. However, little is known about how food preferences can be effectively affected and what neural systems support such changes. In this study, we investigated a novel extensive training paradigm where participants chose from specific pairs of palatable junk food items and were rewarded for choosing the items with lower subjective value over higher value ones. In a later probe phase, when choices were made for real consumption, participants chose the lower-valued item more often in the trained pairs compared with untrained pairs. We replicated the behavioral results in an independent sample of participants while they were scanned with fMRI. We found that, as training progressed, there was decreased recruitment of regions that have been previously associated with cognitive control, specifically the left dorsolateral pFC and bilateral parietal cortices. Furthermore, we found that connectivity of the left dorsolateral pFC was greater with primary motor regions by the end of training for choices of lower-valued items that required exertion of self-control, suggesting a formation of a stronger stimulus-response association. These findings demonstrate that it is possible to influence food choices through training and that this training is associated with a decreasing need for top-down frontoparietal control. The results suggest that training paradigms may be promising as the basis for interventions to influence real-world food preferences.

The effects of aging and Alzheimer's disease on cerebral cortical anatomy: specificity and differential relationships with cognition.

Although both normal aging and Alzheimer's disease (AD) are associated with regional cortical atrophy, few studies have directly compared the spatial patterns and magnitude of effects of these two processes. The extant literature has not addressed two important questions: 1) Is the pattern of age-related cortical atrophy different if cognitively intact elderly individuals with silent AD pathology are excluded? and 2) Does the age- or AD-related atrophy relate to cognitive function? Here we studied 142 young controls, 87 older controls, and 28 mild AD patients. In addition, we studied 35 older controls with neuroimaging data indicating the absence of brain amyloid. Whole-cortex analyses identified regions of interest (ROIs) of cortical atrophy in aging and in AD. Results showed that some regions are predominantly affected by age with relatively little additional atrophy in patients with AD, e.g., calcarine cortex; other regions are predominantly affected by AD with much less of an effect of age, e.g., medial temporal cortex. Finally, other regions are affected by both aging and AD, e.g., dorsolateral prefrontal cortex and inferior parietal lobule. Thus, the processes of aging and AD have both differential and partially overlapping effects on specific regions of the cerebral cortex. In particular, some frontoparietal regions are affected by both processes, most temporal lobe regions are affected much more prominently by AD than aging, while sensorimotor and some prefrontal regions are affected specifically by aging and minimally more by AD. Within normal older adults, atrophy in aging-specific cortical regions relates to cognitive performance, while in AD patients atrophy in AD-specific regions relates to cognitive performance. Further work is warranted to investigate the behavioral and clinical relevance of these findings in additional detail, as well as their histological basis; ROIs generated from the present study could be used strategically in such investigations.

Intrinsic connectivity between the hippocampus and posteromedial cortex predicts memory performance in cognitively intact older individuals.

Coherent fluctuations of spontaneous brain activity are present in distinct functional-anatomic brain systems during undirected wakefulness. However, the behavioral significance of this spontaneous activity has only begun to be investigated. Our previous studies have demonstrated that successful memory formation requires coordinated neural activity in a distributed memory network including the hippocampus and posteromedial cortices, specifically the precuneus and posterior cingulate (PPC), thought to be integral nodes of the default network. In this study, we examined whether intrinsic connectivity during the resting state between the hippocampus and PPC can predict individual differences in the performance of an associative memory task among cognitively intact older individuals. The intrinsic connectivity, between regions within the hippocampus and PPC that were maximally engaged during a subsequent memory fMRI task, was measured during a period of rest prior to the performance of the memory paradigm. Stronger connectivity between the hippocampal and posteromedial regions during rest predicted better performance on the memory task. Furthermore, hippocampal-PPC intrinsic connectivity was also significantly correlated with episodic memory measures on neuropsychological tests, but not with performance in non-memory domains. Whole-brain exploratory analyses further confirmed the spatial specificity of the relationship between hippocampal-default network posteromedial cortical connectivity and memory performance in older subjects. Our findings provide support for the hypothesis that one of the functions of this large-scale brain network is to subserve episodic memory processes. Research is ongoing to determine if impaired connectivity between these regions may serve as a predictor of memory decline related to early Alzheimer's disease.

Intrinsic interhemispheric hippocampal functional connectivity predicts individual differences in memory performance ability.

When given challenging episodic memory tasks, young adults demonstrate notable individual differences in performance. Recent evidence suggests that individual differences in human behavior may be related to the strength of functional connectivity of large-scale functional networks as measured by spontaneous fluctuations in regional brain activity during quiet wakefulness (the "resting state"), in the absence of task performance. In this study, we sought to determine whether individual differences in memory performance could be predicted by the interhemispheric functional connectivity of the two hippocampi, hypothesized to reflect the intrinsic connectivity within the large-scale medial temporal lobe memory system. Results demonstrated that interhemispheric hippocampal functional connectivity during quiet wakefulness was predictive of the capacity to freely recall recently learned information (r = 0.47, P < 0.05). In contrast, functional connectivity of bilateral motor cortices had no relationship to free recall, supporting the specificity of the hippocampal data. Thus, individual differences in the capacity to perform episodic memory tasks, which may be persistent behavioral traits or transient states, may be at least partly subserved by individual differences in the functional connectivity of large-scale functional-anatomic memory networks.

Automated segmentation of hippocampal subfields from ultra-high resolution in vivo MRI.

Recent developments in MRI data acquisition technology are starting to yield images that show anatomical features of the hippocampal formation at an unprecedented level of detail, providing the basis for hippocampal subfield measurement. However, a fundamental bottleneck in MRI studies of the hippocampus at the subfield level is that they currently depend on manual segmentation, a laborious process that severely limits the amount of data that can be analyzed. In this article, we present a computational method for segmenting the hippocampal subfields in ultra-high resolution MRI data in a fully automated fashion. Using Bayesian inference, we use a statistical model of image formation around the hippocampal area to obtain automated segmentations. We validate the proposed technique by comparing its segmentations to corresponding manual delineations in ultra-high resolution MRI scans of 10 individuals, and show that automated volume measurements of the larger subfields correlate well with manual volume estimates. Unlike manual segmentations, our automated technique is fully reproducible, and fast enough to enable routine analysis of the hippocampal subfields in large imaging studies.

The cortical signature of prodromal AD: regional thinning predicts mild AD dementia.

OBJECTIVE: We previously used exploratory analyses across the entire cortex to determine that mild Alzheimer disease (AD) is reliably associated with a cortical signature of thinning in specific limbic and association regions. Here we investigated whether the cortical signature of AD-related thinning is present in individuals with questionable AD dementia (QAD) and whether a greater degree of regional cortical thinning predicts mild AD dementia. METHODS: Participants included 49 older adults with mild impairment consistent with mild cognitive impairment (Clinical Dementia Rating [CDR] = 0.5) at the time of structural MRI scanning. Cortical thickness was measured in nine regions of interest (ROIs) identified previously from a comparison of patients with mild AD and controls. RESULTS: Longitudinal clinical follow-up revealed that 20 participants converted to mild AD dementia (progressors) while 29 remained stable (nonprogressors) approximately 2.5 years after scanning. At baseline, QAD participants showed a milder degree of cortical thinning than typically seen in mild AD, and CDR Sum-of-Boxes correlated with thickness in temporal and parietal ROIs. Compared to nonprogressors, progressors showed temporal and parietal thinning. Using receiver operating characteristic curves, the thickness of an aggregate measure of these regions predicted progression to mild AD with 83% sensitivity and 65% specificity. CONCLUSIONS: Thinning in specific cortical areas known to be affected by Alzheimer disease (AD) is detectable in individuals with questionable AD dementia (QAD) and predicts conversion to mild AD dementia. This method could be useful for identifying individuals at relatively high risk for imminent progression from QAD to mild AD dementia, which may be of value in clinical trials.

The cortical signature of Alzheimer's disease: regionally specific cortical thinning relates to symptom severity in very mild to mild AD dementia and is detectable in asymptomatic amyloid-positive individuals.

Alzheimer's disease (AD) is associated with neurodegeneration in vulnerable limbic and heteromodal regions of the cerebral cortex, detectable in vivo using magnetic resonance imaging. It is not clear whether abnormalities of cortical anatomy in AD can be reliably measured across different subject samples, how closely they track symptoms, and whether they are detectable prior to symptoms. An exploratory map of cortical thinning in mild AD was used to define regions of interest that were applied in a hypothesis-driven fashion to other subject samples. Results demonstrate a reliably quantifiable in vivo signature of abnormal cortical anatomy in AD, which parallels known regional vulnerability to AD neuropathology. Thinning in vulnerable cortical regions relates to symptom severity even in the earliest stages of clinical symptoms. Furthermore, subtle thinning is present in asymptomatic older controls with brain amyloid binding as detected with amyloid imaging. The reliability and clinical validity of AD-related cortical thinning suggests potential utility as an imaging biomarker. This "disease signature" approach to cortical morphometry, in which disease effects are mapped across the cortical mantle and then used to define ROIs for hypothesis-driven analyses, may provide a powerful methodological framework for studies of neuropsychiatric diseases.