A comparison of visceral and somatic pain processing in the human brainstem using functional magnetic resonance imaging - PubMed (original) (raw)

Comparative Study

A comparison of visceral and somatic pain processing in the human brainstem using functional magnetic resonance imaging

Paul Dunckley et al. J Neurosci. 2005.

Abstract

Evidence from both human and animal studies has demonstrated a key role for brainstem centers in the control of ascending nociceptive input. Nuclei such as the rostral ventromedial medulla and periaqueductal gray (PAG) are able to both inhibit and facilitate the nociceptive response. It has been proposed that altered descending modulation may underlie many of the chronic pain syndromes (both somatic and visceral). We used functional magnetic resonance imaging to image the neural correlates of visceral and somatic pain within the brainstem. Ten healthy subjects were scanned twice at 3 tesla, during which they received matched, moderately painful, electrical stimuli to either the midline lower abdomen or rectum. Significant activation was observed in regions consistent with the PAG, nucleus cuneiformis (NCF), ventral tegmental area/substantia nigra, parabrachial nuclei/nucleus ceruleus, and red nucleus bilaterally to both stimuli. Marked spatial similarities in activation were observed for visceral and somatic pain, although significantly greater activation of the NCF (left NCF, p = 0.02; right NCF, p = 0.01; Student's paired t test, two-tailed) was observed in the visceral pain group compared with the somatic group. Right PAG activity correlated with anxiety during visceral stimulation (r = 0.74; p < 0.05, Pearson's r, two-tailed) but not somatic stimulation. We propose that the differences in NCF and right PAG activation observed may represent a greater nocifensive response and greater emotive salience of visceral over somatic pain.

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Figures

Figure 1.

Figure 1.

Graphical representation of the slice orientation during the functional scan. For clarity, the underlying image is a T1-weighted structural scan, and the number of slices was reduced from 24 to 8. A coronal-oblique orientation was used with slices aligned with the ventral wall of the fourth ventricle.

Figure 2.

Figure 2.

Axial slices through a PDTSE sequence structural scan of the brainstem. These were designed to provide maximal resolution and contrast within the brainstem to aid accurate region of interest mask formation. The substantia nigra (SN) and PAG are seen in lighter contrast. The red nucleus (RN), dentate nucleus (DN), decussation of the corticospinal tracts (DCST), and inferior olivary nucleus (ION) are labeled.

Figure 3.

Figure 3.

The group psychophysical data. The stimuli were well matched, with no significant differences in either intensity or unpleasantness rating between visceral or somatic stimulation (p > 0.05; Student's t test, paired, two-tailed). Electrical stimulation of the rectum induced a mild urge sensation. Error bars represent SE.

Figure 4.

Figure 4.

Group activation maps for somatic (first column) and visceral (second column) pain. The sagittal slices show columns of activation within the brainstem in each group. Axial slices (a-e) correspond to the plane indicated in the sagittal slice. A reduced field of view was used during functional scanning; thus, the activation map is limited in its anteroposterior plane. The two groups have a similar spatial pattern of activation. Regions commonly activated in whole-brain pain-imaging studies are significantly activated: thalamus (Thal) and posterior insula (Ins) bilaterally. Activation was also seen in the globus pallidus (GP) bilaterally in both groups. Significantly, activated brainstem nuclei included the red nucleus (RN), NCF, PAG, VTA [which extended laterally into the substantia nigra (SN)], and the dorsolateral pons (DLPons) bilaterally. Bilateral activation of the PN occurred in the visceral group but was limited to the right side in the somatic group. Activation in the region of the RVM was also seen in both groups. In the visceral group alone, a region of activation occurred in the left dorsolateral medulla (DLM). A small area of motion artifact (MA) occurred around the central canal in the somatic group. The axial slices in the visceral group have been magnified and juxtaposed to drawings at the same anatomical location [modified from Duvernoy (1995) with permission].

Figure 5.

Figure 5.

Nucleus cuneiformis activity. Significantly greater activation occurred bilaterally in the NCF during visceral pain (*p < 0.05; Student's t test, two-tailed, paired, uncorrected). Error bars represent SE.

Figure 6.

Figure 6.

Correlation of anxiety with PAG activity during visceral pain. a, The mean PAG parameter estimate for visceral and somatic pain; no significant difference in activation was observed. a, b, Anxiety during the painful visceral stimuli correlated with right (R) PAG activity (b; r = 0.74; p < 0.05; Pearson's r, two-tailed) and approached significance for the left (L) PAG (a; r = 0.66; p = 0.08; Pearson's r, two-tailed).

Figure 7.

Figure 7.

Correlation analysis between RVM activity and that of the dorsolateral pons in the region of the PBN and NC (PBN-NC). A significant correlation was seen bilaterally for visceral stimulation (a, b) (right, r = 0.65, p = 0.04; left, r = 0.75, p = 0.01; Pearson's r, two-tailed) but not for somatic stimulation (c, d) (right, r = 0.51, p = 0.13; left, r = 0.75, p = 0.03; Pearson's r, two-tailed). R, Right; L, left.

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