Regional differences in the sympathetic innervation of the Guinea pig large intestine by neuropeptide Y- and tyrosine hydroxylase-immunoreactive nerves of divergent extrinsic origin

Browning, Kirsteen N.; Cunningham, Shauna M. C.; Duncan, Linda; Timmermans, Jean‐Pierre; Lees, G.J.

doi:10.1002/(sici)1096-9861(19990809)410:4<515::aid-cne1>3.0.co;2-5

Cited by 12 publications

(8 citation statements)

References 31 publications

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“…Similarly, sympathetic axon terminals within the smooth muscle, particularly within the circular muscle sheets, became varicose as they formed long, parallel arrays within the muscle layer. Consistent with previous reports for rats (Phillips et al, 2006), mice (Tan et al, 2009), and guinea-pigs (Furness and Costa, 1974; Browning et al, 1999), TH-IR axons and terminals were not observed, in the present study, within the serosa or subserosal layer(s) of the adult rat small intestine.…”

Section: Discussionsupporting

confidence: 93%

Sympathetic axonopathies and hyperinnervation in the small intestine smooth muscle of aged Fischer 344 rats

Phillips

Hudson

Powley

2013

Autonomic Neuroscience

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It is well documented that the intrinsic enteric nervous system of the gastrointestinal (GI) tract sustains neuronal losses and reorganizes as it ages. In contrast, age-related remodeling of the extrinsic sympathetic projections to the wall of the gut is poorly characterized. The present experiment, therefore, surveyed the sympathetic projections to the aged small intestine for axonopathies. Furthermore, the experiment evaluated the specific prediction that catecholaminergic inputs undergo hyperplastic changes. Jejunal tissue was collected from 3-, 8-, 16-, and 24-month-old male Fischer 344 rats, prepared as whole mounts consisting of the muscularis, and processed immunohistochemically for tyrosine hydroxylase, the enzymatic marker for norepinephrine, and either the protein CD163 or the protein MHCII, both phenotypical markers for macrophages. Four distinctive sympathetic axonopathy profiles occurred in the small intestine of the aged rat: (1) swollen and dystrophic terminals, (2) tangled axons, (3) discrete hyperinnervated loci in the smooth muscle wall, including at the bases of Peyer's patches, and (4) ectopic hyperplastic or hyperinnervating axons in the serosa/subserosal layers. In many cases, the axonopathies occurred at localized and limited foci, involving only a few axon terminals, in a pattern consistent with incidences of focal ischemic, vascular, or traumatic insult. The present observations underscore the complexity of the processes of aging on the neural circuitry of the gut, with age-related GI functional impairments likely reflecting a constellation of adjustments that range from selective neuronal losses, through accumulation of cellular debris, to hyperplasias and hyperinnervation of sympathetic inputs.

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Section: Discussionsupporting

confidence: 93%

Sympathetic axonopathies and hyperinnervation in the small intestine smooth muscle of aged Fischer 344 rats

Phillips

Hudson

Powley

2013

Autonomic Neuroscience

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“…To the best of our knowledge, this is the first direct comparison between stretch-sensitive rectal and colonic PN afferents. Whereas the rectal component of the large bowel in humans is anatomically distinguished as the segment distal to the sigmoidal colon (29), the distinction between the rodent rectum and distal colon is relatively subtle (8), as both are contained in the final straight segment of the bowel. Histologically, the human rectum features the merger of flat bands of muscle into a continuous outer longitudinal muscle layer (29) thicker than the smooth muscle layer in the distal colon, and this seems to be preserved in rodent species as well (see Fig.…”

Section: Discussionmentioning

confidence: 99%

Differential roles of stretch-sensitive pelvic nerve afferents innervating mouse distal colon and rectum

Feng

Brumovsky

Gebhart

2010

American Journal of Physiology-Gastrointestinal and Liver Physi

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Feng B, Brumovsky PR, Gebhart GF. Differential roles of stretchsensitive pelvic nerve afferents innervating mouse distal colon and rectum. Am J Physiol Gastrointest Liver Physiol 298: G402-G409, 2010. First published January 14, 2010; doi:10.1152/ajpgi.00487.2009.-Information about colorectal distension (i.e., colorectal dilation by increased intraluminal pressure) is primarily encoded by stretch-sensitive colorectal afferents in the pelvic nerve (PN). Despite anatomic differences between rectum and distal colon, little is known about the functional roles of colonic vs. rectal afferents in the PN pathway or the quantitative nature of mechanosensory encoding. We utilized an in vitro mouse colorectum-PN preparation to investigate pressure-encoding characteristics of colorectal afferents. The colorectum with PN attached was dissected, opened longitudinally, and pinned flat in a Sylgard-lined chamber. Action potentials of afferent fibers evoked by circumferential stretch (servo-controlled force actuator) were recorded from the PN. Stretch-sensitive fibers were categorized into the following four groups: colonic muscular, colonic muscular/mucosal, rectal muscular, and rectal muscular/mucosal. Seventy-nine stretchsensitive PN afferents evenly distributed into the above four groups were studied. Rectal muscular afferents had significantly greater stretch-responses than the other three groups. Virtually all rectal afferents (98%) had low thresholds for response and encoded stimulus intensity into the noxious range without obvious saturation. Most colonic afferents (72%) also had low thresholds (Ͻ14 mmHg), but a significant proportion (28%) had high thresholds (Ͼ18 mmHg) for response. These high-threshold colonic afferents were sensitized to stretch by inflammatory soup; response threshold was significantly reduced (from 23 to 12 mmHg), and response magnitude significantly increased. These results suggest that the encoding of mechanosensory information differs between colonic and rectal stretch-sensitive PN afferents. Rectal afferents have a wide response range to stretch, whereas high-threshold colonic afferents likely contribute to visceral nociception. muscular afferents; muscular/mucosal afferents; single-fiber recording; irritable bowel syndrome FUNCTIONAL GASTROINTESTINAL DISORDERS such as irritable bowel syndrome (IBS) are characterized by altered bowel habits, discomfort, pain, and colorectal hypersensitivity (12). Typically, patients have significantly lower response thresholds to provocative visceral stimuli (e.g., distension of hollow organs) and complain of increased sensitivity and discomfort to ingestion of food or beverages (16). Balloon distension of the pelvic colorectum has been widely employed to quantify sensation (principally discomfort and pain) in patients with IBS as a means of assessing colorectal hypersensitivity relative to normal subjects (e.g., Ref.3). Growing evidence from both clinical and basic science research reveals that peripheral sensory input plays a key role in sustaining visceral p...

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“…SOM immunoreactivity never surrounded submucosal arterioloes, whereas dense innervation of arterioles by NPY-IR and CGRP-IR varicose processes was evident, although these two markers were never colocalised in varicosities around arterioles. The NPY-IR periarterial fibres are probably sympathetic vasoconstrictor axons (Messenger and Furness 1990;Browning et al 1999). NPY immunoreactivity was present in 85% of SOM-IR neurons, although all NPY-IR neurons were SOM-IR, which indicates that SOM-IR may be present in a subgroup of either ACh/calretinin or ACh/TK/calbindin neurons (Fig.…”

Section: Submucosal Plexusmentioning

confidence: 92%

Neurochemical classification of enteric neurons in the guinea-pig distal colon

Lomax

Furness

2000

Cell and Tissue Research

185

240

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Previous studies have identified the chemistries, shapes, projections and electrophysiological characteristics of several populations of neurons in the distal colon of the guinea-pig but it is unknown how these characteristics correlate to define the classes of neurons present. We have used double-label immunohistochemical techniques to identify neurochemically distinct subgroups of enteric neurons in this region. On the basis of colocalisation of neurochemical markers and knowledge gained from previous studies of neural projections, 17 classes of neurons were identified. The myenteric plexus contained the cell bodies of 13 distinct types of neurons. Four classes of descending interneurons and three classes of ascending interneurons were identified, together with inhibitory and excitatory motor neurons to both the circular and longitudinal muscle layers. Dogiel type II neurons, which are presumed to be intrinsic primary afferent neurons, were located in myenteric and submucosal ganglia; they were all immunoreactive for choline acetyltransferase and often calbindin and tachykinins. Three classes of secretomotor neurons with cell bodies in submucosal ganglia were defined. Two of these classes were immunoreactive for choline acetyltransferase and the other class was immunoreactive for both vasoactive intestinal peptide and nitric oxide synthase. Some of the secretomotor neurons probably also have a vasomotor function. The neural subtypes defined in the present study are similar in many respects to those found in the small intestine, although differences are evident, especially in populations of interneurons. These differences presumably reflect the differing physiological roles of the two intestinal regions.

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Regional differences in the sympathetic innervation of the Guinea pig large intestine by neuropeptide Y- and tyrosine hydroxylase-immunoreactive nerves of divergent extrinsic origin

Cited by 12 publications

References 31 publications

Sympathetic axonopathies and hyperinnervation in the small intestine smooth muscle of aged Fischer 344 rats

Sympathetic axonopathies and hyperinnervation in the small intestine smooth muscle of aged Fischer 344 rats

Differential roles of stretch-sensitive pelvic nerve afferents innervating mouse distal colon and rectum

Neurochemical classification of enteric neurons in the guinea-pig distal colon

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