As the gut ages: Timetables for aging of innervation vary by organ in the Fischer 344 rat

Abstract

To explore the effects of aging on the vagal innervation of the gastrointestinal (GI) tract, male Fischer 344 rats at 3 and 24 months of age were injected in the left nodose ganglion with 3 microl of either 4% wheat germ agglutinin-horseradish peroxidase (to label sensory endings) or 1% cholera toxin subunit B-horseradish peroxidase (to label motor endings). The stomach and duodenum were prepared as wholemounts and processed with tetramethyl benzidine. In addition, to study age-related changes in the myenteric plexus, the stomachs, small intestines, and large intestines from 3-, 12-, 21-, 24- and 27-month-old rats were prepared as wholemounts and processed with Cuprolinic Blue (to stain the neurons). Vagal afferent endings, motor terminal profiles, and myenteric neurons were counted and mapped with a sampling grid. In the stomach, both the vagal and myenteric innervation were stable between the ages of 3 and 24 months; however, a decrease in the number of myenteric neurons in the forestomach was noted at 27 months. In the small and large intestines, myenteric cell loss occurred by 12 months of age, progressed with age, and appeared to be governed by several general principles: (1) the rate of cell loss was organ-specific, with a gradient of increasing severity from proximal to distal in the gut; (2) within organs of the GI tract, the rate of cell loss differed between regions; and (3) for given regions, cell losses progressed linearly with increasing age. The findings suggest that a positive relationship exists between the density of vagal extrinsic innervation and myenteric neuron survival; however, whether this results from the vagal innervation and/or other factor(s) protecting or rescuing myenteric neurons from age-related attrition remains to be determined.

Administering ascorbic acid to rats undergoing ageing processes: effects on myosin-V immunoreactive myenteric neurons

“…It is considered that neuronal loss with age would be accompanied by a rearrangement of the remaining elements; as such, it could not be regarded as a degenerative process, as the remaining ganglionic elements would have greater efficiency (Santer and Baker 1988). Similar results were obtained by other authors (Phillips and Powley 2001); however, they believe that neurodegeneration continues linearly throughout life.…”

“…MELLO et al changes in the morphology and density of ENS neurons, influencing GIT functioning (Hansen 2003, Phillips andPowley 2007). Neurodegeneration in the myenteric plexus is a characteristic of ageing observed in rodents (Saffrey and Burnstock 1994, Phillips and Powley 2001, Phillips et al 2003Thrasivoulou 2006), with an approximate reduction of 50% in the neuron population for rats between 3 and 30 months of age (Gabella 1996, Phillips andPowley 2007). However, the life stage in which this loss begins is still questioned.…”

Effect of aging on regional cerebral blood flow responses associated with osmotic thirst and its satiation by water drinking: A PET study

“…The presence or absence of aging effects on the innervation and function of the stomach could be critical for the satiation process in older people. At a structural level, the aging stomach is more notable for decreasing levels of sympathetic innervation than for loss of afferent fibers (23,24). Motor responses in the stomach are likely to influence the passage of water through the gut, and consequently age associated sympathetic fiber loss could effect the accurate coding of water volume in the stomach.…”

Age-Related Changes of Calbindin D-28k-Immunoreactive Neurons in the Myenteric Plexus of Gerbil Duodenum

“…The immunohistochemical localization of these substances has been important for the analysis of the neuronal circuitry of the ENS [5,6,40]. It has been reported that the neuronal loss in the gastrointestinal tract of the rat starts in early adulthood and continues in a roughly linear manner over the rodent's lifespan [36][37][38][39].…”