Spatial Tuning in Nociceptive Processing Is Driven by Attention

Abstract

When the source of nociception expands across a body area, the experience of pain increases due to the spatial integration of nociceptive information. This well-established effect is called spatial summation of pain (SSp) and has been the subject of multiple investigations. Here, we used cold-induced SSp to investigate the effect of attention on the spatial tuning of nociceptive processing. Forty pain-free volunteers (N = 40, 20 females) participated in this experiment. They took part in an SSp paradigm based on three hand immersions into cold water (5°C): Participants either immersed the radial segment ("a"), ulnar segment ("b") or both hand segments ("a+b") and provided overall pain ratings. In some trials based on "a+b" immersions, they were also asked to provide divided (ie, first pain in "a" then in "b"; or reversed) and directed attention ratings (ie, pain only in "a" or "b"). Results confirmed a clear SSp effect in which reported pain during immersions of "a" or "b" was less intense than pain during immersions of "a+b" (P < .001). Data also confirmed that spatial tuning was altered. SSp was abolished when participants provided two ratings in a divided fashion (P < .001). Furthermore, pain was significantly lower when attention was directed only to one segment ("a" OR "b") during "a+b" immersion (P < .001). We conclude that spatial tuning is dynamically driven by attention as reflected in abolished SSp. Directed attention was sufficient to focus spatial tuning and abolish SSp. Results support the role of cognitive processes such as attention in spatial tuning. PERSPECTIVE: This article presents experimental investigation of spatial tuning in pain and offers mechanistic insights of contiguous spatial summation of pain in healthy volunteers. Depending on how pain is evaluated in terms of attentional derivative (overall pain, directed, divided attention) the pain is reduced and spatial summation abolished.

Keywords: Spatial summation; Troxler fading; attentional modulation; cold pressor; pain; receptive field; spatial tuning.

Figure 1.. Spatial summation of pain paradigm.

Segments of the hand exposed to noxious cold stimulation are presented in blue. The hand was divided into two equal segments (see trial 1), i.e., “a” (radial) and “b” (ulnar). The border dividing the hand into segments was marked on the skin. Participants immersed either two segments simultaneously (“a+b”, trials: 1, 4–7) or just one of them (“a” or “b”, trials 2–3). Overall pain ratings were obtained from both segments (1), only the ulnar (2) or radial (3) segment. Directed attention ratings were obtained from radial (4) and ulnar (5) segments. Divided attention ratings were obtained sequentially such that the first rating from “a” then “b” (trials 6) or in a reversed fashion (trial 7). These trials were presented in two pseudorandom blocks with block I using the trial order of 3-4-1-6-2-7-5 and block II using the trial order 5-1-6-2-4-3-7.

Figure 2.. Spatial summation of pain was abolished in the divided attention condition.

The horizontal axis includes experimental conditions, and the type of stimuli is marked with colors: Cyan, immersions of segments “a” or “b” alone, dark blue, immersions of segments “a+b”. A clear spatial summation effect was observed when contrasting pain from stimulation of 2 segments (“a+b”) vs. just one segment (“a” or “b”). Note that the spatial summation was fully abolished when ratings were collected in a divided fashion, e.g., first “a” then “b” (“a|b” or reversed). Dots refer to individual data points, horizontal black lines depict mean values. P-values are presented following correction: ***p< 0.001.

Figure 3.. Magnitude of examined effects expressed as relative (%) change in pain.

Left panel (summation): Pain increased by 25% during whole hand immersions compared to just one segment. Right panel (attentional effects): Pain decreased by 10% in directed attention ratings and by 14% in divided attention ratings (14%) compared to overall ratings.

Figure 4.. Directed attention diminished experienced pain intensity.

The horizontal axis includes experimental conditions, and the type of stimuli is marked with colors: Cyan, immersions of segments “a” or “b” alone, blue, immersions of segments “a+b”. Note that pain was significantly lowered when the two segments were immersed, and participants directed their attention only to one segment of the hand (“a” or “b”). Even though the stimulation area was doubled in these immersions, the pain did not significantly differ from ratings during immersion of only one segment. Dots refer to individual data points, horizontal black lines depict mean values. P-values are presented following correction: ***p< 0.001, **p< 0.01.