The Neuroanatomical Correlates of Visceral Pain: An Activation Likelihood Estimation Meta-Analysis
Abstract
1. Introduction
2. Methods
2.1. Data Sources and Search Strategy
2.2. Eligibility Criteria
2.3. Study Selection and Quality Assessment
2.4. Data Extraction and Statistical Analysis
3. Results
3.1. Study Selection
3.2. ALE Cluster Analysis
Scheme | Population | Intervention | ||||
---|---|---|---|---|---|---|
Author (Year) | Study Design | Imaging Modality | Sample Size (% Female) | Mean Age ± SD (Years) | Conditions | Foci |
Strigo et al. (2003) [20] | Prospective experimental study | 1.5 T fMRI | 7 (43%) | 25.8 range 19–34 | Esophageal balloon distension with the balloon catheter positioned 5 cm above the lower esophageal sphincter; cutaneous heat stimulation onto the upper midline chest; two stimulus intensities low/high; stimuli were presented three times in a counter-balanced and quasi-randomized order. | 24 |
Verne et al. (2003) [21] | Prospective experimental study | 1.5 T fMRI | 9 (67%) | 29 ± 9 | Phasic rectal balloon distension to pressures of 35 mmHg or 55 mmHg for 20 s with 20 s interstimulus control period for cycles; cutaneous pain tested with a heated water bath at three temperatures (35, 45, 47 °C); pain rating on a VAS; psychological tests with BDI, Somatic Focus (PILL), STAI, State-Trait Anger Expression Inventory, Coping Strategies Questionnaire, and the NEO-FFI. | 5 |
Lu et al. (2004) [22] | Prospective experimental study | 3 T fMRI | 10 (20%) | 23.6 | Gastric fundus distension with an air inflated balloon; conditions of either non-painful or painful gastric distension (60–70% on a VAS rating scale); psychological test with STAI, BDI, NEO-FFI. | 48 |
Andresen et al. (2005) [23] | Prospective experimental study | 1.5 T fMRI | 8 (63%) | 41.3 range 27–64 | Rectal balloon distensions of subliminal, liminal, and supraliminal stimulation intensities adapted to the individual perception threshold; perception rating from 1 to 6, each distension lasted for 20 s followed by a rest of 10 s. | 12 |
Ladabaum et al. (2006) [24] | Prospective experimental study | 1.5 T fMRI | 18 (78%) | 32 ± 6.5 | Gastric balloon distension sequences of ten 45 s isobaric inflations to gastric sensation of ≥6 and <9 on a VAS scale; sequences of 45 s deflations to minimal distending pressure. | 39 |
Hui-Song et al. (2006) [25] | Prospective experimental study | 3 T fMRI | 12 (100%) | 23.0 | Rectal balloon distension with a pressure of 20% above the pain detection threshold; foot cold pressor test with an ice water bath at 4 °C, rating on a 5-points scale. | 15 |
Berman et al. (2008) [26] | Prospective experimental study | 1.5 T fMRI | 15 (100%) | 36.3 ± 7.3 | Rectal balloon distension, four to six stimulus sets containing 16 trials with pressures of 5, 25 or 45 mmHg. | 22 |
Study ID | Population | Intervention | ||||
---|---|---|---|---|---|---|
Author (Year) | Study Design | Imaging Modality | Sample Size (% Female) | Mean Age ± SD (Years) | Conditions | Foci |
Coen et al. (2009) [27] | Prospective experimental study | 1.5 T fMRI | 12 (0%) | 26.0 21–31 | Esophageal balloon catheter inflated to produce 40 trials of either painful or non-painful sensations; stimulation was performed under neutral or negative emotions. | 11 |
Elsenbruch et al. (2009) [28] | Prospective experimental study | 1.5 T fMRI | 12 (100%) | 31.4 ± 2.3 | Rectal balloon distension, staircase increments of 2–10 mmHg until a subjective threshold of 5 on a 6-point scale was reached; ratings on HADS, STAI-S, and SCL-90-R. | 6 |
Moisset et al. (2010) [29] | Prospective experimental study | 1.5 T fMRI | 11 (100%) | 38.4 ± 3.1 | Rectal balloon distension until a subjective threshold of either 2 (non-painful stimulus) or 5 (painful stimulus) on a 6-point scale; psychological test with PAS and short-form McGill questionnaire. | 21 |
Lu et al. (2010) [30] | Prospective experimental study | 3 T fMRI | 14 (64%) | 23.9 ± 3.9 | Esophageal balloon distension until 60–70% of subjective pain intensity, administration of normal saline during control condition; during placebo conditions, participants were told to receive an opioid intravenously; ratings on PCS, VAS, and McGill pain questionnaire. | 27 |
Benson et al. (2011) [31] | Prospective experimental study | 1.5 T fMRI | 30 (50%) | 25.75 ± 6.1 | Rectal balloon distensions until an individual pain threshold of 5 on a 6 points scale; eight phases of distension alternated with eight phases without distension and a duration of 31 s for each condition; auditory cue before distension to assess anticipation; rating with HADS and VAS. | 17 |
Geeraerts et al. (2011) [39] | Prospective experimental study | PET | 14 (29%) | 26.3 ± 1.8 | Gastric fundus balloon distension and continuous and stepwise infusion until individualized abdominal discomfort threshold; comparison between intragastric volumes of balloon distension and continuous or stepwise meal infusion; rating on satiation or upper abdominal sensation scale. | 6 |
Smith et al. (2011) [32] | Prospective experimental study | 3 T fMRI | 14 (100%) | n.a. | Rectal balloon distension; five repetitions of four conditions consisting of no stimulus, subliminal stimulus, liminal stimulus and painful stimulus for 40 s each; rating with HAD, PHQ-15, and VAS. | 34 |
Study ID | Population | Intervention | ||||
---|---|---|---|---|---|---|
Author (Year) | Study Design | Imaging Modality | Sample Size (% Female) | Mean Age ± SD (Years) | Conditions | Foci |
Schmid et al. (2013) [33] | Prospective experimental study | 3 T fMRI | 36 (50%) | 29.7 ± 1.8 | Rectal balloon distention until a subjective pain threshold between 5 and 6 on 6-point scale; two groups of intravenous infusion of saline/spasmolytic drug (placebo) or saline/opioid antagonist (nocebo); investigation of anticipated effect; rating on HADS, BDI and baseline cortisol levels. | 15 |
Theysohn et al. (2014) [34] | Prospective experimental study | 3 T fMRI | 30 (50%) | 34.7 ± 3.2 | Rectal balloon distension until an individualized pain threshold following a visual stimulus, counterbalanced by visually cued resting periods; participants were told that they would receive an analgesic drug or an inert substance; rating on a VAS scale. | 10 |
Gramsch et al. (2014) [35] | Prospective experimental study | 3 T fMRI | 24 (54%) | 28.8 ± 8.5 | Rectal balloon distension, conditioning paradigm with visual cues to measure distension and anticipation-related neural activation; pain threshold set at subjective pain rating between 5 and 6 on a 6-point scale; ratings on VAS and HADS. | 11 |
Icenhour et al. (2016) [36] | Prospective experimental study | 3 T fMRI | 40 (53%) | 26.00 ± 3.27 range 20–32 | Rectal balloon distensions of high or low intensity paired with visual cues to assess pain and anticipation-related neural activation; pain threshold defined as low intensity for a rating of 4 and high intensity between 5 and 6 on a 6-point scale; rating on VAS, HADS, and STAI. | 6 |
Tanaka et al. (2016) [40] | Prospective experimental study | PET | 16 (0%) | 22.8 ± 2.5 | Rectal balloon distensions at mild (20 mmHg), intense (40 mmHg) compared to baseline and no distension (0 mmHg); effect of CRH or saline intravenously on brain activation was assessed; plasma ACTH, serum cortisol and plasma noradrenaline levels at each stimulation. | 12 |
Guleria et al. (2017) [37] | Prospective experimental study | 3 T fMRI | 10 (0%) | 28.5 range 26.5–31.5 | Rectal balloon distensions to an individualized pain threshold; comparison between healthy controls and patients with IBS. | 5 |
Icenhour et al. (2021) [38] | Prospective experimental study | 3 T fMRI | 27 (44%) | 25.7 ± 1.0 | Rectal balloon distensions in different visual contexts; interoceptive cues were followed by visceral pain as conditioned stimulus; ratings on VAS, HADS, TICS, and STAI. | 22 |
Cluster | Brain Region | BA | x | y | z | Volume (mm3) | ALE (×10−3) |
---|---|---|---|---|---|---|---|
1 | Right Insula | 13 | 41 | 11 | 3 | 7024 | 27.0 |
2 | Left Insula | 13 | −36 | 9 | 7 | 6080 | 37.5 |
3 | Right Thalamus | - | 16 | −16 | 6 | 3592 | 30.1 |
4 | Left Thalamus | - | −11 | −14 | 6 | 2944 | 30.1 |
5 | Right Inferior Parietal Lobe | 40 | 57 | −28 | 29 | 2648 | 26.2 |
6 | Left Postcentral Gyrus | 40 | −62 | −24 | 23 | 1592 | 23.1 |
7 | Right Cingulate Cortex | 32 | 4 | 14 | 41 | 1344 | 16.4 |
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
ACC | Anterior cingulate cortex |
ALE | Activation likelihood estimation |
BA | Brodmann area |
fMRI | Functional magnetic resonance imaging |
FWHM | Full width half maximum |
IBS | Irritable bowel syndrome |
MNI | Montreal Neurological Imaging |
PCC | Posterior cingulate cortex |
PRISMA | Preferred Reporting Items for Systematic Reviews and Meta-Analyses |
VMA | Visceromotor areas |
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Müller, C.; Maxeiner, H. The Neuroanatomical Correlates of Visceral Pain: An Activation Likelihood Estimation Meta-Analysis. Brain Sci. 2025, 15, 651. https://doi.org/10.3390/brainsci15060651
Müller C, Maxeiner H. The Neuroanatomical Correlates of Visceral Pain: An Activation Likelihood Estimation Meta-Analysis. Brain Sciences. 2025; 15(6):651. https://doi.org/10.3390/brainsci15060651
Chicago/Turabian StyleMüller, Christoph, and Hagen Maxeiner. 2025. "The Neuroanatomical Correlates of Visceral Pain: An Activation Likelihood Estimation Meta-Analysis" Brain Sciences 15, no. 6: 651. https://doi.org/10.3390/brainsci15060651
APA StyleMüller, C., & Maxeiner, H. (2025). The Neuroanatomical Correlates of Visceral Pain: An Activation Likelihood Estimation Meta-Analysis. Brain Sciences, 15(6), 651. https://doi.org/10.3390/brainsci15060651