Expectation influences the interruptive function of pain: Behavioural and neural findings.

BACKGROUND: Expectations can dramatically influence the perception of pain, as has been shown in placebo analgesia or nocebo hyperalgesia. Here, we investigated the role of expectation on the interruptive function of pain - the negative consequences of pain on cognitive task performance - in 42 healthy human subjects. METHODS: Verbal and written instructions were used to manipulate the subjects' expectation of how pain would influence their task performance in an established visual categorization task which was performed with or without concomitant painful thermal stimulation during 3T fMRI scanning. The categorization task was followed by a surprise recognition task. RESULTS: We observed a significant interaction between stimulation (pain/no pain) and expectancy (positive expectation/negative expectation): categorization accuracy decreased during painful stimulation in the negative expectancy group (N = 21), while no difference was observed in the positive expectancy group (N = 21). On the neural level, the positive expectancy group showed stronger activity in the anterior cingulate cortex (ACC) and hippocampus during painful stimulation compared to the negative group. Moreover, we detected a decrease in connectivity between ACC and fusiform gyrus during painful stimulation in the negative expectancy group, which was absent in the positive expectancy group. CONCLUSION: Taken together, our data show that expectation can modulate the effect of pain on task performance and that these expectancy effects on the interruptive function of pain are mediated by activity and connectivity changes in brain areas involved in pain processing and task performance. The possibility of changing cognitive task performance by verbal information in clinical population warrants further investigation. SIGNIFICANCE: We show that the interruptive function of pain on concurrent visual task performance is influenced by expectation. Positive expectation can abolish the detrimental effects of pain on cognition. These expectancy effects on the interruptive function of pain are mediated by changes in functional connectivity between rostral ACC, posterior fusiform cortex and the hippocampus.

The differential effect of trigeminal vs. peripheral pain stimulation on visual processing and memory encoding is influenced by pain-related fear.

Compared to peripheral pain, trigeminal pain elicits higher levels of fear, which is assumed to enhance the interruptive effects of pain on concomitant cognitive processes. In this fMRI study we examined the behavioral and neural effects of trigeminal (forehead) and peripheral (hand) pain on visual processing and memory encoding. Cerebral activity was measured in 23 healthy subjects performing a visual categorization task that was immediately followed by a surprise recognition task. During the categorization task subjects received concomitant noxious electrical stimulation on the forehead or hand. Our data show that fear ratings were significantly higher for trigeminal pain. Categorization and recognition performance did not differ between pictures that were presented with trigeminal and peripheral pain. However, object categorization in the presence of trigeminal pain was associated with stronger activity in task-relevant visual areas (lateral occipital complex, LOC), memory encoding areas (hippocampus and parahippocampus) and areas implicated in emotional processing (amygdala) compared to peripheral pain. Further, individual differences in neural activation between the trigeminal and the peripheral condition were positively related to differences in fear ratings between both conditions. Functional connectivity between amygdala and LOC was increased during trigeminal compared to peripheral painful stimulation. Fear-driven compensatory resource activation seems to be enhanced for trigeminal stimuli, presumably due to their exceptional biological relevance.

Experimental pain impairs recognition memory irrespective of pain predictability.

BACKGROUND: Pain is hardwired to signal threat and tissue damage and therefore automatically attracts attention to initiate withdrawal or defensive behaviour. This well-known interruptive function of pain interferes with cognitive functioning and is modulated by bottom-up and top-down variables. Here, we applied predictable or unpredictable painful heat stimuli simultaneously to the presentation of neutral images to investigate (I) whether the predictability of pain modulated its effect on the encoding of images (episodic memory) and (II) whether subjects remember that certain images have been previously presented with pain (source memory). METHODS: Twenty-four healthy subjects performed a categorization task in which 80 images had to be categorized into living or non-living objects. We compared the processing and encoding of these images during cued and non-cued pain trials as well as cued and non-cued pain-free trials. Effects on recognition performance and source memory for pain were immediately tested using a surprise recognition task. RESULTS: Painful thermal stimulation impaired recognition accuracy (d', recollection, familiarity). This negative effect of pain was positively correlated with the individual expectation of pain interference and the attentional avoidance of pain-related words. However, the interruptive effect of pain was not modulated by the predictability of pain. Source memory for painful stimulation was at chance level, indicating that subjects did not explicitly remember that images had been paired with pain. CONCLUSIONS: Targeting negative expectations and a maladaptive attentional bias for pain-related material might help reducing frequently reported pain-induced cognitive impairments.