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Unexpected Omissions of Threat Trigger Reward-Like Signaling and Subjective Relief in the Human Brain


Core Concepts
Unexpected omissions of threat trigger activations in key regions of the reward and salience pathways, such as the ventral tegmental area/substantia nigra, that partially fit the profile of a positive reward prediction error signal. These neural responses are linked to the subjective experience of pleasurable relief.
Abstract
The study examined how the brain processes unexpected omissions of threat and how this relates to the subjective experience of relief. The authors used an Expectancy Violation Assessment (EVA) task, where participants received instructions about the probability and intensity of an upcoming electrical stimulation, which was then sometimes omitted. The key findings are: Unexpected omissions of threat triggered increased activations in the ventral tegmental area/substantia nigra (VTA/SN), ventral putamen, anterior insula, and dorsomedial prefrontal cortex/anterior midcingulate cortex. These activations partially fit the profile of a positive reward prediction error (PE) signal, as they increased with the probability and intensity of the omitted threat. In contrast, the nucleus accumbens showed no change in activation, while the ventromedial prefrontal cortex showed deactivations that increased with the intensity of the omitted threat. The magnitude of the VTA/SN, ventral putamen, and deactivations in the ventromedial prefrontal cortex correlated with the subjective pleasantness of the relief experienced during threat omissions. A data-driven multivariate analysis identified a distributed pattern of brain responses across multiple regions that could predict the subjective relief experienced, suggesting the experience of relief may not be confined to a single brain region. Overall, the results provide evidence that unexpected omissions of threat trigger reward-like prediction error signals in the human brain, which are linked to the subjective experience of relief. This supports the idea that the neural processing of absent danger shares similarities with the processing of unexpected rewards.
Stats
The intensity of the electrical stimulation was calibrated for each participant, with the weak stimulus being "mildly uncomfortable", the moderate stimulus being "very uncomfortable, but not painful", and the strong stimulus being "significantly painful, but tolerable". The selected Weak (M = 9.35 mA, SD = 4.65), moderate (M = 16.26 mA, SD = 8.13), and strong (M = 34.26 mA, SD = 19.53) stimulation intensities differed significantly. Skin conductance responses were larger following omissions of more probable and more intense electrical stimulations. The pleasantness of the relief elicited by omissions was rated as being more pleasant following omissions of more intense and more probable electrical stimulations.
Quotes
"Unexpected (non-0%) omissions of threat elicited higher levels of relief-pleasantness and omission SCR than fully expected omissions (0%)." "Omission-related activations in the VTA/SN, but not striatal or vmPFC activations increased in a PE-like manner." "Omission-related activations in the bilateral aINS and dmPFC/aMCC increased with increasing probability and intensity of omitted threat."

Deeper Inquiries

How do the neural responses to threat omission relate to actual learning and expectancy updating in contexts where the omission is informative for future behavior?

The neural responses to threat omission play a crucial role in learning and expectancy updating, especially in contexts where the omission provides valuable information for future behavior. In fear extinction paradigms, for example, the unexpected omission of a threat serves as a critical signal for safety learning. When a previously threatening cue (CS) is repeatedly presented without the aversive event (US), a new safety association is formed between the CS and the absence of threat. This process involves a prediction error (PE) signal, where the mismatch between the expected threat and its omission leads to the strengthening of the safety association. Neuroscientific studies have shown that regions like the ventral tegmental area/substantia nigra (VTA/SN), nucleus accumbens (NAc), and prefrontal areas are involved in processing threat omission PE signals. These regions are part of the reward and salience pathways and are crucial for encoding the unexpected absence of threat. The VTA/SN, in particular, is known for its role in encoding positive reward PE signals, and studies have shown that its activations increase with the intensity and probability of omitted threat, similar to reward-related PE signals. In learning contexts, the neural responses to threat omission are essential for updating expectancies and guiding future behavior. The activations in these regions reflect the processing of unexpected outcomes and contribute to the formation of safety associations. By studying these neural responses, researchers can gain insights into how the brain learns to distinguish between threat and safety cues, leading to adaptive behavior in the face of potential danger.

How are the observed neural responses to threat omission altered in clinical populations, such as individuals with anxiety disorders, who show impairments in fear extinction learning?

Individuals with anxiety disorders often exhibit impairments in fear extinction learning, which can be linked to alterations in neural responses to threat omission. Studies have shown that individuals with anxiety disorders have dysregulated activity in regions involved in threat processing, such as the amygdala, prefrontal cortex, and striatum. These alterations can lead to difficulties in distinguishing between threatening and safe cues, resulting in persistent fear responses even in the absence of actual threat. In the context of threat omission, individuals with anxiety disorders may show exaggerated responses to the unexpected absence of threat. For example, heightened amygdala activity and reduced prefrontal cortex modulation during threat omission could contribute to the maintenance of fear responses and impairments in fear extinction learning. Additionally, abnormalities in the dopaminergic system, including the VTA/SN and NAc, may impact the processing of threat omission PE signals, further exacerbating fear-related behaviors. Understanding how neural responses to threat omission are altered in clinical populations is crucial for developing targeted interventions for anxiety disorders. By identifying specific neural markers associated with fear extinction deficits, researchers can develop novel treatment strategies that aim to normalize these responses and improve fear learning and extinction in individuals with anxiety disorders.

What are the functional and anatomical distinctions between the VTA/SN responses to salient events versus prediction error signals, and how do they interact in the context of threat omission processing?

The VTA/SN plays a critical role in processing both salient events and prediction error signals, but there are functional and anatomical distinctions between these processes. In the context of salient events, the VTA/SN responds to stimuli that are behaviorally relevant or rewarding, leading to the release of dopamine in target regions like the NAc. This response is crucial for motivating goal-directed behavior and encoding the value of stimuli in the environment. On the other hand, prediction error signals in the VTA/SN are involved in updating expectations based on the outcomes of actions. When an outcome deviates from the predicted value, dopaminergic neurons in the VTA/SN fire in response to the prediction error, signaling a mismatch between expectation and reality. This signal is essential for reinforcement learning and guiding future behavior based on the discrepancy between predicted and actual outcomes. In the context of threat omission processing, the VTA/SN responses to salient events and prediction error signals interact to encode the unexpected absence of threat. When a threatening cue is presented without the aversive event, the VTA/SN generates a prediction error signal that strengthens the safety association. This process involves both the salience of the unexpected omission and the updating of expectations regarding threat and safety cues. Overall, the VTA/SN responses to salient events and prediction error signals work in concert to process threat omission and facilitate safety learning. By integrating information about the salience of threat cues and the prediction errors associated with their omission, the VTA/SN contributes to adaptive responses to potential danger and the formation of safety associations in the brain.
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