Attentional modulation of spatial integration of pain: evidence for dynamic spatial tuning

Abstract

In many sensory modalities, afferent processing is dynamically modulated by attention and this modulation produces altered sensory experiences. Attention is able to alter perceived pain, but the mechanisms involved in this modulation have not been elucidated. To determine whether attention alters spatial integration of nociceptive information, subjects were recruited to evaluate pain from pairs of noxious/innocuous thermal stimuli during different spatial attentional tasks. Divided attention was able to abolish spatial summation and produce inhibition of pain. In contrast, directed attention enhanced pain intensity by partially integrating both stimuli. This dynamic modulation of spatial integration indicates that attention alters spatial dimensions of afferent nociceptive processing to optimize the perceptual response to input from a particular body region or stimulus feature. This dynamic spatial tuning of nociceptive processing provides a new conceptual insight into the functional significance of endogenous pain inhibitory and facilitatory mechanisms.

Figures

Figure 1.

Temporal and quantitative synchronization of stimuli. Stimulus temperatures delivered by each probe were highly similar and were well synchronized (average of 214 paired 49/49°C trials).

Figure 2.

Attention modulates spatial integration of information from two noxious stimuli (mean ± SEM). A, B, During divided attention (div att; 49/49°C and 49/49°C) spatial summation of pain (49/49°C overall) was abolished at distal (49/49°C div att; A) and proximal sites (49/49°C div att; B). This was associated with inhibition when compared with a single 49°C (49 control) at distal stimuli (A) but not at proximal sites (B). The modulation of pain was not attributable to nonspecific attentional effects because during the directed attention (dir att; 49/49°C and 49/49°C) pain ratings were greater than during divided attention at distal (49/49°C div att; A) and proximal (49/49°C div att; B) sites.

Figure 3.

Division of attention produces inhibition of pain (mean ± SEM). A, During the stimulus conditions where proximal probes had a high probability (50%) of being activated (35/49°C and 49/49°C), distal pain ratings were significantly reduced relative to single stimuli and to conditions where the proximal probe had a low probability (0%) of being activated (off/49°C). B, Such reduction in pain ratings was not observed at proximal sites.

Figure 4.

Conceptualization of attentional effects on RF organization and spatial integration of nociceptive information. Left, Spatial distribution of RF of nociceptive neurons innervating the body surface. The x-axis represents the location of the receptive field on the body surface whereas the y-axis represents the sensitivity of that neuron at a given spatial location. Each neuron is numbered in the center of its RF. Vertical dashed lines originate from the center of the RFs of neurons in A to demonstrate RF shifts in B–E. Right, Magnitude of the activation of each individual neuron and the total neuronal population output used for the subjective evaluation of pain. A value of 1 represents the evoked responses from stimulation in the center of the RF (i.e., neuron 1; A). Population outputs were derived from the sum of the neural output of all neurons activated by a given stimulus. If a neuron was activated by both stimuli, its total activity is added to both population outputs. The red square symbolizes the site where subjects were required to pay attention. A, Each individual neuron is represented with a different color. During a single noxious stimulus without any spatial attentional requirement, different activation is found in neurons depending on their RF location in relation to the stimulus. The hypothetical output from the population is ∼2.0. B, When subjects are required to direct their attention to a single noxious stimulus (49 control condition), there is an enhancement of sensitivity inside the target area and a focusing of the RFs that have their centers close to the stimulus. Also the RFs of neurons adjacent to the stimuli (2, 3, and 4) are shifted to the attended area. The neurons far away from the focus of attention (5) have their activity diminished to better contrast between attended and nonattended areas. This pattern of activity is consistent with that predicted by the spotlight/multiplicative enhancement effect (Compte and Wang, 2006). The population output is 2.5. C, Two noxious thermal stimuli are applied simultaneously and subjects are required to direct their attention to only stimulus 1 (49°C/49°C directed attention). As in B, there is enhanced sensitivity inside the target area and diminished sensitivity to the nonattended stimulus. However, some neurons (3) are activated by both stimuli and integrate them. This interaction of neuronal activity can account for the slight increase of pain during the directed attention condition and produces an increase in the population output for stimulus 1 (∼3.0). D, Two noxious thermal stimuli are applied simultaneously and subjects are asked to divide their attention between the two stimuli (49/49°C divided attention). This task requires segregation of information from the two stimuli, so increased surround inhibition is used to create a silent zone in the intermediate area. Also to improve spatial resolution, RF sizes are reduced to better distinguish information from each of the two stimuli. Accordingly, spatial summation of pain is not allowed to occur and inhibition is produced (B vs D). The population output for each stimulus is 1.8. E, Two noxious thermal stimuli are applied simultaneously and subjects are required to integrate pain experience from both stimuli (49/49°C, no spatial attention required, overall ratings). There is no spatial focusing of RF (shrinking around the stimuli), and spatial summation of pain is produced. Accordingly, the population output is 3.2.