Disentangling the roles of dopamine and noradrenaline in the exploration-exploitation tradeoff during human decision-making.

Balancing the exploration of new options and the exploitation of known options is a fundamental challenge in decision-making, yet the mechanisms involved in this balance are not fully understood. Here, we aimed to elucidate the distinct roles of dopamine and noradrenaline in the exploration-exploitation tradeoff during human choice. To this end, we used a double-blind, placebo-controlled design in which participants received either a placebo, 400 mg of the D2/D3 receptor antagonist amisulpride, or 40 mg of the ß-adrenergic receptor antagonist propranolol before they completed a virtual patch-foraging task probing exploration and exploitation. We systematically varied the rewards associated with choice options, the rate by which rewards decreased over time, and the opportunity costs it took to switch to the next option to disentangle the contributions of dopamine and noradrenaline to specific choice aspects. Our data show that amisulpride increased the sensitivity to all of these three critical choice features, whereas propranolol was associated with a reduced tendency to use value information. Our findings provide novel insights into the specific roles of dopamine and noradrenaline in the regulation of human choice behavior, suggesting a critical involvement of dopamine in directed exploration and a role of noradrenaline in more random exploration.

Prediction Errors for Aversive Events Shape Long-Term Memory Formation through a Distinct Neural Mechanism.

Prediction errors (PEs) have been known for decades to guide associative learning, but their role in episodic memory formation has been discovered only recently. To identify the neural mechanisms underlying the impact of aversive PEs on long-term memory formation, we used functional magnetic resonance imaging, while participants saw a series of unique stimuli and estimated the probability that an aversive shock would follow. Our behavioral data showed that negative PEs (i.e., omission of an expected outcome) were associated with superior recognition of the predictive stimuli, whereas positive PEs (i.e., presentation of an unexpected outcome) impaired subsequent memory. While medial temporal lobe (MTL) activity during stimulus encoding was overall associated with enhanced memory, memory-enhancing effects of negative PEs were linked to even decreased MTL activation. Additional large-scale network analyses showed PE-related increases in crosstalk between the "salience network" and a frontoparietal network commonly implicated in memory formation for expectancy-congruent events. These effects could not be explained by mere changes in physiological arousal or the prediction itself. Our results suggest that the superior memory for events associated with negative aversive PEs is driven by a potentially distinct neural mechanism that might serve to set these memories apart from those with expected outcomes.

On the search for a selective and retroactive strengthening of memory: Is there evidence for category-specific behavioral tagging?

Storing motivationally salient experiences preferentially in long-term memory is generally adaptive. Although such relevant experiences are often immediately obvious, a problem arises when the relevance of initially ambiguous events becomes evident sometime after encoding. Is there a mechanism that enables the retroactive enhancement of specific memories? Recent evidence suggests the existence of such a mechanism that selectively strengthens weak memories for neutral stimuli from one category when their respective category gains motivational significance later. Although such a selective retroactive memory enhancement has considerable implications for adaptive memory, evidence for this phenomenon is based on only few studies. Here, we report data from four attempts to replicate category-specific retroactive memory enhancements for neutral stimuli from a category that was later predictive of aversive electric shocks. Although our data showed enhanced memory for the arousing stimuli themselves as well as related subsequent stimuli, none of our experiments provided any evidence for category-specific retroactive memory enhancement when strictly replicating the analysis strategy from the original study. In an additional analysis focusing on high confidence memory only, one of four experiments indicated a significant retroactive memory effect but only in corrected recognition and not in d' based on signal detection theory. In an analysis pooled across all experiments, we found a small but significant retroactive memory effect again solely for high-confidence corrected recognition, although the corresponding Bayesian analysis indicated even substantial evidence for the null hypothesis. Overall, our data cast doubt on the reliability and generalizability of the proposed selective retroactive enhancement of initially weak memory. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

How representative are neuroimaging samples? Large-scale evidence for trait anxiety differences between fMRI and behaviour-only research participants.

Over the past three decades, functional magnetic resonance imaging (fMRI) has become crucial to study how cognitive processes are implemented in the human brain. However, the question of whether participants recruited into fMRI studies differ from participants recruited into other study contexts has received little to no attention. This is particularly pertinent when effects fail to generalize across study contexts: for example, a behavioural effect discovered in a non-imaging context not replicating in a neuroimaging environment. Here, we tested the hypothesis, motivated by preliminary findings (N = 272), that fMRI participants differ from behaviour-only participants on one fundamental individual difference variable: trait anxiety. Analysing trait anxiety scores and possible confounding variables from healthy volunteers across multiple institutions (N = 3317), we found robust support for lower trait anxiety in fMRI study participants, consistent with a sampling or self-selection bias. The bias was larger in studies that relied on phone screening (compared with full in-person psychiatric screening), recruited at least partly from convenience samples (compared with community samples), and in pharmacology studies. Our findings highlight the need for surveying trait anxiety at recruitment and for appropriate screening procedures or sampling strategies to mitigate this bias.

Stress reduces both model-based and model-free neural computations during flexible learning.

Stressful events are thought to impair the flexible adaptation to changing environments, yet the underlying mechanisms are largely unknown. Here, we combined computational modeling and functional magnetic resonance imaging (fMRI) to elucidate the neurocomputational mechanisms underlying stress-induced deficits in flexible learning. Healthy participants underwent a stress or control manipulation before they completed, in the MRI scanner, a Markov decision task, frequently used to dissociate model-based and model-free contributions to choice, with repeated reversals of reward contingencies. Our results showed that stress attenuated the behavioral sensitivity to reversals in reward contingencies. Computational modeling further indicated that stress specifically affected the use of value computations for subsequent action selection. This reduced application of learned information on subsequent behavior was paralleled by a stress-induced reduction in inferolateral prefrontal cortex activity during model-free computations. For model-based learning, stress decreased specifically posterior, but not anterior, hippocampal activity, pointing to a functional segregation of model-based processing and its modulation by stress along the hippocampal longitudinal axis. Our findings shed light on the mechanisms underlying deficits in flexible learning under stress and indicate that, in highly dynamic environments, stress may hamper both model-based and model-free contributions to adaptive behavior.

Expectancy Violation Drives Memory Boost for Stressful Events.

Stressful events are often vividly remembered. Although generally adaptive to survival, this emotional-memory enhancement may contribute to stress-related disorders. We tested here whether the enhanced memory for stressful events is due to the expectancy violation evoked by these events. Ninety-four men and women underwent a stressful or control episode. Critically, to manipulate the degree of expectancy violation, we gave participants either detailed or minimal information about the stressor. Although the subjective and hormonal stress responses were comparable in informed and uninformed participants, prior information about the stressor abolished the memory advantage for core features of the stressful event, tested 7 days later. Using functional near-infrared spectroscopy, we further linked the expectancy violation and memory formation under stress to the inferior temporal cortex. These data are the first to show that detailed information about an upcoming stressor and, by implication, a reduced expectancy violation attenuates the memory for stressful events.

Beyond arousal: Prediction error related to aversive events promotes episodic memory formation.

Stimuli encoded shortly before an aversive event are typically well remembered. Traditionally, this emotional memory enhancement has been attributed to beneficial effects of physiological arousal on memory formation. Here, we proposed an additional mechanism and tested whether memory formation is driven by the unpredictable nature of aversive events (i.e., aversive prediction errors). In a combined Pavlovian fear conditioning and incidental memory paradigm, participants saw initially neutral pictures from 2 distinct categories, 1 of which was associated with a risk to receive an electric shock. During encoding, we measured both physiological arousal and explicit prediction errors to explain memory differences in a surprise recognition test that followed approximately 24 hr later. In a first experiment, we show that physiological arousal, expressed as outcome-related skin conductance responses, was associated with improved recognition memory, corroborating arousal-based models. Critically, unsigned binary prediction errors derived from explicit shock expectancy ratings in each trial were also linked to enhanced recognition and model fits showed that the impact of prediction errors on memory was dissociable from the impact of arousal. In a second experiment, we replicated and extended the findings of the first experiment by demonstrating that the memory-promoting effect of prediction errors remained even after controlling for arousal. The present data point to prediction error-related learning as a cognitive mechanism that contributes to the emotional enhancement of memory, above and beyond the well-established effects of arousal in emotional memory formation. (PsycINFO Database Record (c) 2020 APA, all rights reserved).