Frontoparietal mechanisms supporting attention to location and intensity of painful stimuli

Abstract

Attention can profoundly shape the experience of pain. However, little is known about the neural mechanisms that support directed attention to nociceptive information. In the present study, subjects were cued to attend to either the spatial location or the intensity of sequentially presented pairs of painful heat stimuli during a delayed match-to-sample discrimination task. We hypothesized that attention-related brain activation would be initiated after the presentation of the attentional cue and would be sustained through the discrimination task. Conjunction analysis confirmed that bilateral portions of the posterior parietal cortex (intraparietal sulcus [IPS] and superior parietal lobule) exhibited this sustained activity during attention to spatial but not intensity features of pain. Analyses contrasting activation during spatial and intensity attention tasks revealed that the right IPS region of the posterior parietal cortex was consistently more activated across multiple phases of the spatial task. However, attention to either feature of the noxious stimulus was associated with activation of frontoparietal areas (IPS and frontal eye fields) as well as priming of the primary somatosensory cortex. Taken together, these results delineate the neural substrates that support selective amplification of different features of noxious stimuli for utilization in discriminative processes.

Keywords: Attention; Imaging; Pain; Parietal; fMRI.

Figure 1

The temporal sequence of the discrimination task. Ten seconds before T1, a sound cue instructed subjects to attend to either the location or intensity of the stimulus. Noxious stimuli (T1 and T2) were then delivered sequentially for 20 seconds each with an interstimulus (memory) interval of 30 seconds. Before the end of T2, subjects had to indicate whether T2 was different (or same) from T1 in location or intensity depending on the cue. The period between the end of the cue and beginning of T1 was considered the cue maintenance period. The discrimination period was defined as the first 75% of the time interval between the beginning of T2 and subject’s response. The corresponding time period in T1 was defined as acquisition period. Thus, regressors for the acquisition and discrimination period were unique for every discrimination pair.

Figure 2

Behavioral responses during spatial and intensity discriminations (mean ± SEM). Difference 1 corresponds to the smaller difference either in location (4 cm) or intensity (1°C). Difference 2 corresponds to the larger difference in location (16 cm) or intensity (2°C). Both error rates (*, p = 0.0038) and response latencies (*, p< 0.0001) were significantly lower for spatial compared to intensity discriminations. As location or temperature differences between T1 and T2 stimuli decreased, response latencies and error rates became significantly larger, indicating that discrimination of noxious heat stimuli became more difficult. Although performance on catch trials varied between spatial and intensity tasks, the magnitude of the increase in the error rates between “catch” and “same” trials was almost identical between the two.

Figure 3

Brain activations and deactivations during painful heat stimulations (T1 and T2 periods). Noxious stimuli produced activation in thalamus, putamen, caudate, insula, SI and SII, as well as deactivations in PCC, precuneus and VMPFC. Slice locations are relative to standard Montreal Neurologic Institute (MNI) stereotaxic space.

Figure 4

Brain activations and deactivations during cue maintenance period. Conjunction analysis of spatial and intensity cue maintenance periods detected common activations in the cerebellum, hippocampus, FEF, IPS and SI. These activations are consistent with retrieval of cue meaning, top-down attentional engagement and priming of early somatosensory areas. The spatial task produced greater activation in right IPS. Slice locations are relative to standard MNI stereotaxic space.

Figure 5

Brain activations and deactivations during the acquisition period. Conjunction analysis did not detect any clusters of overlapping activity during the spatial and intensity acquisition periods. The spatial task produced greater activation in right SPL, IPS and FEF. Activity in these areas likely represents top-down attention to the stimulus, as well as engagement of the dorsal stream of sensory information processing. Intensity task produced greater activation in LOC. Slice locations are relative to standard MNI stereotaxic space.

Figure 6

Brain activations and deactivations during the memory period. Conjunction analysis of activation during the spatial and intensity memory periods detected clusters of overlapping activity in the cerebellum, OFC, insula, frontal operculum, and left IPS. The spatial task produced greater activation in the right insula, DLPFC as well as ACC. Slice locations are relative to standard MNI stereotaxic space.

Figure 7

Brain activations and deactivations during discrimination period. Conjunction analysis of spatial and intensity discrimination periods detected clusters of overlapping activity in bilateral thalamus, caudate, putamen, insula, ACC, OFC, DLPFC, frontal operculum, IPS, as well as left paracentral lobule. The spatial task produced greater activation in SII, ACC, FEF, and PPC. Intensity discrimination produced greater activity in cerebellum, and left DLPFC. Slice locations are relative to standard MNI stereotaxic space.

Figure 8

Clusters of overlapping activity between cue maintenance, acquisition, and discrimination periods in spatial task as detected by conjunction analysis. Bilateral regions of IPS and SPL were active not only during orientation of attention (cue maintenance period), but also maintained their activity during stimulus presentation (acquisition and discrimination periods). Slice locations are relative to standard MNI stereotaxic space.