Controlling attention to nociceptive stimuli with working memory

Abstract

Background: Because pain often signals the occurrence of potential tissue damage, a nociceptive stimulus has the capacity to involuntarily capture attention and take priority over other sensory inputs. Whether distraction by nociception actually occurs may depend upon the cognitive characteristics of the ongoing activities. The present study tested the role of working memory in controlling the attentional capture by nociception.

Methodology and principal findings: Participants performed visual discrimination and matching tasks in which visual targets were shortly preceded by a tactile distracter. The two tasks were chosen because of the different effects the involvement of working memory produces on performance, in order to dissociate the specific role of working memory in the control of attention from the effect of general resource demands. Occasionally (i.e. 17% of the trials), tactile distracters were replaced by a novel nociceptive stimulus in order to distract participants from the visual tasks. Indeed, in the control conditions (no working memory), reaction times to visual targets were increased when the target was preceded by a novel nociceptive distracter as compared to the target preceded by a frequent tactile distracter, suggesting attentional capture by the novel nociceptive stimulus. However, when the task required an active rehearsal of the visual target in working memory, the novel nociceptive stimulus no longer induced a lengthening of reaction times to visual targets, indicating a reduction of the distraction produced by the novel nociceptive stimulus. This effect was independent of the overall task demands.

Conclusion and significance: Loading working memory with pain-unrelated information may reduce the ability of nociceptive input to involuntarily capture attention, and shields cognitive processing from nociceptive distraction. An efficient control of attention over pain is best guaranteed by the ability to maintain active goal priorities during achievement of cognitive activities and to keep pain-related information out of task settings.

Figure 1. Experimental trials.

The experiment started with a grey fixation cross that was present at the center of the screen (black background) during the entire stimulation block. Each trial started with a somatosensory stimulus. Somatosensory stimulus was either a 0.5-ms tactile electrocutaneous pulse applied over the left nervus radialis or a 50-ms laser nociceptive pulse applied to the left hand dorsum. Each somatosensory stimulus was followed by a visual stimulus presented briefly during 500 ms and consisting of two 6-cm circles at 4.9° left and right from the fixation cross. The color of the circles was blue (RGB 0*0*255) and/or yellow (RGB 255*255*0). The inter-stimulus time interval (ISI) between the onset of the somatosensory stimulus and the onset of the visual stimulus was 220 ms when the somatosensory stimulus was tactile, and 300 ms when it was nociceptive. The inter-trial time interval (ITI) was 3000 ms measured between the onsets of visual stimuli. Participants were asked to respond to the color of the visual stimuli. Performance was measured within the time window running from 150 to 1500 ms after visual stimulus onset.

Figure 2. Experimental paradigm.

(a) During one of the two sessions, participants were involved in a color discrimination task in which they had to respond according to the color of each visual stimulus constituted of two circles that were either both yellow or both blue. In the 0-back condition, they responded according to the color of the current stimulus. In the 1-back condition, they responded according to the color to the stimulus that was presented one trial before. (b) During the other session, participants performed a color matching task in which they had to respond according to whether the colors of two targets were matched or unmatched. In the 0-back condition, they compared the color of the two circles of the current stimulus, which were matched (yellow-yellow, blue-blue) or unmatched (yellow-blue, blue-yellow). In the 1-back condition, they compared the color of the current stimulus (yellow-yellow, blue-blue) to the color of the preceding stimulus (yellow-yellow, blue-blue). Note that only the 0-back matching task contained stimulus in which colors of the two circles could be different. The visual targets were preceded by a tactile stimulus in 83% of trials, or by a nociceptive stimulus in the remaining 17% of trials.

Figure 3. Response accuracy.

Percentage of errors to the visual targets according to the task (discrimination vs. matching), the engagement of working memory (0-back vs. 1-back) and the type of somatosensory distracter (novel nociceptive vs. standard tactile). Error bars represent confidence intervals .

Figure 4. Response speeds.

(a) Mean reaction times (RTs) to the visual targets (in milliseconds) according to the task (discrimination vs. matching), the engagement of working memory (0-back vs. 1 back) and the type of somatosensory distracter (novel nociceptive vs. standard tactile). Error bars represent confidence intervals . (b) Distraction indexes assessed by subtracting the mean RTs to the visual targets that followed a standard tactile distracter from the mean RTs to the visual targets that followed a novel nociceptive distracter. Error bars represent standard deviations.