A Comparison of Visceral and Somatic Pain Processing in the Human Brainstem Using Functional Magnetic Resonance Imaging

Dunckley, Paul; Wise, Richard G.; Fairhurst, Merle T.; Hobden, Peter; Aziz, Qasim; Chang, Lin; Tracey, Irene

doi:10.1523/jneurosci.1100-05.2005

Cited by 240 publications

(177 citation statements)

References 66 publications

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“…This suggests that the vlPAG maybe involved in these processes and would certainly tie in with the hindbrain connectivity seen, relating to anxiety and aversion processing. Interestingly, these findings correlate with human fMRI studies of visceral and somatic pain processing [Dunckley et al, 2005], where correlation between PAG activation and anxiety was observed during visceral pain (vlPAG processed) but not during somatic pain (dlPAG processes).…”

Section: Discussionsupporting

confidence: 82%

Connectivity‐based segmentation of the periaqueductal gray matter in human with brainstem optimized diffusion MRI

Ezra

Faull

Jbabdi

et al. 2015

Human Brain Mapping

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The periaqueductal gray matter (PAG) is a midbrain structure, involved in key homeostatic neurobiological functions, such as pain modulation and cardiorespiratory control. Animal research has identified four subdivisional columns that differ in both connectivity and function. Until now these findings have not been replicated in humans. This study used high‐resolution brainstem optimized diffusion magnetic resonance imaging and probabilistic tractography to segment the human PAG into four subdivisions, based on voxel connectivity profiles. We identified four distinct subdivisions demonstrating high spatial concordance with the columns of the animal model. The resolution of these subdivisions for individual subjects permitted detailed examination of their structural connectivity without the requirement of an a priori starting location. Interestingly patterns of forebrain connectivity appear to be different to those found in nonhuman studies, whereas midbrain and hindbrain connectivity appears to be maintained. Although there are similarities in the columnar structure of the PAG subdivisions between humans and nonhuman animals, there appears to be different patterns of cortical connectivity. This suggests that the functional organization of the PAG may be different between species, and as a consequence, functional studies in nonhumans may not be directly translatable to humans. This highlights the need for focused functional studies in humans. Hum Brain Mapp 36:3459–3471, 2015. © 2015 The Authors Human Brain Mapping Published by Wiley Periodicals, Inc.

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Section: Discussionsupporting

confidence: 82%

Connectivity‐based segmentation of the periaqueductal gray matter in human with brainstem optimized diffusion MRI

Ezra

Faull

Jbabdi

et al. 2015

Human Brain Mapping

View full text Add to dashboard Cite

show abstract

“…RVM on-cells are directly inhibited by opioids, and it is suggested that these cells express mu-opioid receptors [38]. Moreover, increased RVM neuronal responses to noxious stimuli observed in human imaging studies indicate on-cell activity [39,40]. Therefore, we suggest that decreased responses in the RVM observed in the present study reflect inhibited on-cell activity through the AAR system activation.…”

Section: Discussionsupporting

confidence: 55%

The Neural Basis of Self-Touch in a Pain-Free Situation

Kikuchi¹,

Shirato²,

Machida³

et al. 2018

Neuropsychiatry

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Objective:Self-touch is thought to be an act of coping with harmful or stressful situations, based on the mechanism which suppresses somatosensory perception as well as somatosensory cortex activity, and sympathetic activity. In addition, this suppression can be observed in even nonpainful and non-stressful situations. However, its detailed neural mechanism remains unknown. Several studied have shown, not only that the descending pain modulatory system (DPMS) plays critical roles in painful situations, but also that there is intrinsic functional connectivity in the DPMS in even non-painful situations. Based on these findings, we hypothesized that the neural system consisting of the anterior cingulate cortex (ACC), amygdala and rostral ventromedial medulla (RVM) would play a basic role in self-touch, and we here investigated interactive effects of these regions in a pain-free self-touch situation. Methods:We used functional magnetic resonance imaging (fMRI) to investigate brain activity induced by mere self-touch (rubbing the left hand with the right) in a pain-free and stress-free situation, and carried out the Physio-Physiological Interaction (PPI) analysis to investigate the modulatory effects of brain activity. Results:PPI analysis showed that the rostral ACC (rACC) modulated activity in the RVM and left cerebellum (CB) via the right amygdala, such that the modulation linearly suppressed RVM and left CB activity. Furthermore, the latter was positively correlated with right primary somatosensory cortex (SI) activity. Moreover, we also showed that coherent activity in the bilateral secondary somatosensory cortex (SII) modulated activity of both the left temporoparietal junction (TPJ) and RVM, with the latter also suppressed by the modulation in a linear fashion. Conclusion:These findings suggest that self-touch exerts inhibitory effects on sensory afferents and sympathetic activity through the ACC-amygdala-RVM (AAR) system, and that bilateral sensorimotor integration plays an important role in the effect based on the bodily self.

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“…In addition to its modulating influence on pain (Dunckley et al, 2005), the PAG, through opioidergic mechanisms, suppresses respiration (Sessle et al, 1981) via direct actions on the nucleus tractus solitarius in the ventral lateral medulla. The PAG is connected to the prefrontal cortex (Hadjipavlou et al, 2006), in which we have identified breath hold-related BOLD signal decreases.…”

Section: Opioid-sensitive Aspects Of the Breath Holdmentioning

confidence: 99%

Opioids Depress Cortical Centers Responsible for the Volitional Control of Respiration

Pattinson¹,

Governo²,

MacIntosh³

et al. 2009

Journal of Neuroscience

157

138

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Respiratory depression limits provision of safe opioid analgesia and is the main cause of death in drug addicts. Although opioids are known to inhibit brainstem respiratory activity, their effects on cortical areas that mediate respiration are less well understood. Here, functional magnetic resonance imaging was used to examine how brainstem and cortical activity related to a short breath hold is modulated by the opioid remifentanil. We hypothesized that remifentanil would differentially depress brain areas that mediate sensoryaffective components of respiration over those that mediate volitional motor control. Quantitative measures of cerebral blood flow were used to control for hypercapnia-induced changes in blood oxygen level-dependent (BOLD) signal. Awareness of respiration, reflected by an urge-to-breathe score, was profoundly reduced with remifentanil. Urge to breathe was associated with activity in the bilateral insula, frontal operculum, and secondary somatosensory cortex. Localized remifentanil-induced decreases in breath hold-related activity were observed in the left anterior insula and operculum. We also observed remifentanil-induced decreases in the BOLD response to breath holding in the left dorsolateral prefrontal cortex, anterior cingulate, the cerebellum, and periaqueductal gray, brain areas that mediate task performance. Activity in areas mediating motor control (putamen, motor cortex) and sensory-motor integration (supramarginal gyrus) were unaffected by remifentanil. Breath hold-related activity was observed in the medulla. These findings highlight the importance of higher cortical centers in providing contextual awareness of respiration that leads to appropriate modulation of respiratory control. Opioids have profound effects on the cortical centers that control breathing, which potentiates their actions in the brainstem.

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A Comparison of Visceral and Somatic Pain Processing in the Human Brainstem Using Functional Magnetic Resonance Imaging

Cited by 240 publications

References 66 publications

Connectivity‐based segmentation of the periaqueductal gray matter in human with brainstem optimized diffusion MRI

Connectivity‐based segmentation of the periaqueductal gray matter in human with brainstem optimized diffusion MRI

The Neural Basis of Self-Touch in a Pain-Free Situation

Opioids Depress Cortical Centers Responsible for the Volitional Control of Respiration

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