Characterization of the primary spinal afferent innervation of the mouse colon using retrograde labelling

Robinson, D. K.; McNaughton, Peter A.; Evans, Marcus; Hicks, Gareth A.

doi:10.1046/j.1365-2982.2003.00456.x

Cited by 182 publications

(203 citation statements)

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“…As expected and in agreement with existing literature (Jancso and Maggi 1987;Robinson et al 2004;Wang et al 1998;Zhong et al 2003), most bladder afferents projected from the L6-S1 DRG in both rodents, while a smaller, but still notable, population was present in TL DRG. In our studies, the distribution of retrogradelylabeled distal colon afferents also paralleled that of the bladder and, in general, was in agreement with the bimodal LS and TL peaks as noted in the Wistar rat (Vizzard et al 2000) and C57Bl/6 mice (Christianson et al 2006b;Robinson et al 2004). In support of the specificity of our labeling studies, dually-labeled cells were identified only at DRG levels that have previously been shown to contain both distal colon and urinary bladder afferents (Christianson et al 2006b;de Groat et al 1987;Keast and De Groat 1992;Robinson et al 2004).…”

Section: Discussionsupporting

confidence: 92%

“…In our studies, the distribution of retrogradelylabeled distal colon afferents also paralleled that of the bladder and, in general, was in agreement with the bimodal LS and TL peaks as noted in the Wistar rat (Vizzard et al 2000) and C57Bl/6 mice (Christianson et al 2006b;Robinson et al 2004). In support of the specificity of our labeling studies, dually-labeled cells were identified only at DRG levels that have previously been shown to contain both distal colon and urinary bladder afferents (Christianson et al 2006b;de Groat et al 1987;Keast and De Groat 1992;Robinson et al 2004). Further supporting the specificity of our findings, bladder denervation substantially reduced labeling of bladder afferents and consequentially the number of dually-labeled cells.…”

Section: Discussionsupporting

confidence: 89%

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Convergence of bladder and colon sensory innervation occurs at the primary afferent level

Christianson¹,

Liang²,

Ustinova³

et al. 2007

Pain

177

155

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Dichotomizing afferents are individual dorsal root ganglion (DRG) neurons that innervate two distinct structures thereby providing a form of afferent convergence that may be involved in pelvic organ cross-sensitization. To determine the distribution of dichotomizing afferents supplying the distal colon and bladder of the Sprague-Dawley rat and the C57Bl/6 mouse, we performed concurrent retrograde labeling of urinary bladder and distal colon afferents using cholera toxin subunit B (CTB) fluorescent conjugates. Animals were perfused 4-5 days after sub-serosal organ injections, and the T10-S2 DRG were removed, sectioned, and analyzed using confocal microscopy. In the rat, CTBpositive afferents retrogradely labeled from the bladder were nearly 3 times more numerous than those labeled from the distal colon, while in the mouse, each organ was equally represented. In both species, the majority of colon and bladder afferents projected from lumbosacral (LS) ganglia and secondarily from thoracolumbar (TL) ganglia. In the rat, 17% of the total CTB-positive neurons were retrogradely labeled from both organs with 11% localized in TL, 6% in LS, and 0.8% in thoracic (TH) ganglia. In the mouse, 21% of the total CTB-positive neurons were dually-labeled with 12% localized in LS, 4% in TH, and 4% in TL ganglia. These findings support the existence of dichotomizing pelvic afferents, which provide a pre-existing neuronal substrate for possible immediate and maintained pelvic organ cross-sensitization and ultimately may play a role in the overlap of pelvic pain disorders.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionsupporting

confidence: 89%

Convergence of bladder and colon sensory innervation occurs at the primary afferent level

Christianson¹,

Liang²,

Ustinova³

et al. 2007

Pain

177

155

View full text Add to dashboard Cite

show abstract

“…Dorsal Root Ganglia (DRG) from L6-S1 corresponds to the spinal level for the pelvic innervation of the colo-rectum (Hughes et al, 2007;Robinson et al, 2004). We found that L6-S1 DRG express MOR mRNA (Figure 3Bi), and this expression is substantially increased in L6-S1 DRG from CVH mice when compared to healthy mice (figure 3Bii).…”

Section: Pbmc Supernatants Inhibit Muscular / Mucosal Afferents In CVmentioning

confidence: 91%

Immune derived opioidergic inhibition of viscerosensory afferents is decreased in Irritable Bowel Syndrome patients

Hughes

Moretta

Lim

et al. 2014

Brain, Behavior, and Immunity

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Immune derived opioidergic inhibition of viscerosensory afferents is decreased in Irritable Bowel Syndrome patients, Brain, Behavior, and Immunity (2014), doi: http://dx.doi.org/10. 1016/j.bbi.2014.07.001 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. supernatants from HS and IBS patients were applied to colo-rectal sensory afferent endings in mice with post-inflammatory chronic visceral hypersensitivity (CVH). β-endorphin was identified predominantly in monocyte / macrophages relative to T or B cells in human PBMC and colonic lamina propria. Monocyte derived β-endorphin levels and colonic macrophage numbers were lower in IBS patients than healthy subjects. PBMC supernatants from healthy subjects had greater inhibitory effects on colo-rectal afferent mechanosensitivity than those from IBS patients. The inhibitory effects of PBMC supernatants were more prominent in CVH mice compared to healthy mice due to an increase in µ-opioid receptor expression in dorsal root ganglia neurons in CVH mice. Monocyte / macrophages are the predominant immune cell type responsible for β-endorphin secretion in humans. IBS patients have lower monocyte derived β-endorphin levels than healthy subjects, causing less inhibition of colonic afferent endings. Consequently, altered immune function contributes toward visceral hypersensitivity in IBS.

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“…It is abundant in peptidergic thoracolumbar vascular afferents, 113,114 and is detectable in the majority of their perivascular, intramuscular, ganglionic and mucosal axons in the gut wall. 115 TrpV1 might be directly activated by the acidosis that accompanies frank tissue damage 116 or by local increases in temperature during inflammation.…”

Section: Trp Channels In Vascular Afferentsmentioning

confidence: 99%

Extrinsic primary afferent signalling in the gut

Brookes

Spencer

Costa

et al. 2013

Nat Rev Gastroenterol Hepatol

246

216

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Visceral sensory neurons activate reflex pathways that control gut function and also give rise to important sensations, such as fullness, bloating, nausea, discomfort, urgency and pain. Sensory neurons are organised into three distinct anatomical pathways to the central nervous system (vagal, thoracolumbar and lumbosacral). Although remarkable progress has been made in characterizing the roles of many ion channels, receptors, and second messengers in visceral sensory neurons, the basic aim of understanding how many classes there are, and how they differ, has proven difficult to achieve. We suggest that there are just five structurally distinct types of sensory endings in the gut wall that account for essentially all of the primary afferent neurons in the three pathways. Each of these five major structural types of endings seems to show distinctive combinations of physiological responses. These types are: 'intraganglionic laminar' endings in myenteric ganglia; 'mucosal' endings located in the subepithelial layer; 'muscular mucosal' afferents, with mechanosensitive endings close to the muscularis mucosae; 'intramuscular' endings, with endings within the smooth muscle layers; and 'vascular' afferents, with sensitive endings primarily on blood vessels. 'Silent' afferents might be a subset of inexcitable 'vascular' afferents, which can be switched on by inflammatory mediators.Extrinsic sensory neurons comprise an attractive focus for targeted therapeutic intervention in a range of gastrointestinal disorders.2

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Characterization of the primary spinal afferent innervation of the mouse colon using retrograde labelling

Cited by 182 publications

References 50 publications

Convergence of bladder and colon sensory innervation occurs at the primary afferent level

Convergence of bladder and colon sensory innervation occurs at the primary afferent level

Immune derived opioidergic inhibition of viscerosensory afferents is decreased in Irritable Bowel Syndrome patients

Extrinsic primary afferent signalling in the gut

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