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Location and characterization of the myenteric plexus of insectivorous bats of the species Molossus rufus
Abstract
Bats, from the Molossidae family, are found on all continents. Molossus rufus, are found in Brazil, having an insectivorous feeding habit. The present study aimed to characterize and locate the myenteric plexus in the gastrointestinal tract of Molossus rufus bats from the northwest region of the state of Paraná. Necropsy of five male specimens was performed and the structures corresponding to the stomach and intestines were fixed in 10% neutral buffered formalin for histological preparation of the material, and 0.5cm of each segment was followed for identification of myenteric ganglia using the technique of Giemsa and the histochemistry of NADPH-diaphorase. The myenteric plexus is found between the circular and longitudinal strata of the tunica muscularis, with neurons gathered in ganglia surrounded by bundles of collagen fibers. The ganglia observed in the membrane preparations were formed by different numbers of neurons, interconnected by bundles of nerve fibers, where isolated neurons could be observed. The location of the myenteric plexus found in bats of the species Molossus rufus is similar to those found in other mammals.
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There are no studies that characterize the enteric nervous system (ENS) bats. The organization and density of myenteric neurons may vary according to the animal species, as well as the segment of the digestive tube considered. The nitric oxide is one of the key neurotransmitters present in the myenteric neurons, acting as a mediator in the smooth muscle relaxation. These neurons are evidenced by immunohistochemistry of nitric oxide synthase (NOS) or by NADPH-diaphorase histochemistry. In this sense, this study aimed to characterize the total neuronal population and subpopulation NADPH-d+ of the myenteric plexus present in the jejunum of the insectivore species Molossus rufus quantitatively. Five specimens were collected of M. rufus in a buffer area of the “Reserva Biológica das Perobas” in the microregion of Cianorte/PR. After the euthanasia, in a chamber saturated with isoflurane, segments were collected from the small intestine corresponding to the jejunum intended for two techniques for neuronal marking, Giemsa and NADPH-diaphorase, and a fragment to the histological technique of hematoxylin-eosin and Masson’s trichrome. All the procedures were approved by the “Comitê de Ética no Uso de Animais Unipar” (CEUA - protocol No. 34347/2017) and the “Instituto Chico Mendes de Conservação da Biodiversidade” (ICMBio - protocol No. 60061-1) The histological sections allowed to highlight the location of the myenteric plexus between the longitudinal and circular layers of the muscular tunic. The myenteric plexus had an average of total neuronal population (neurons Giemsa+) of 279.23 neurons/mm2, being the nitrergic neurons (neurons NADPH-d+) represented 20.4% of this total population, with an average of 58.14 neuron/mm2. Therefore, the collected data are consistent with previous studies in other mammalian species concerning the location of the myenteric plexus, as well as the neural myenteric proportion NADPH-d+ compared with the population of neurons Giemsa+. The gaps in the knowledge of ENS of bats limits comparative intraspecific and interspecific studies.
The myenteric plexus has a regular characteristic morphological pattern for each segment of the digestive tube and for each species of animal. Considering the lack of data pertaining to the mentioned plexus in rats of Holtzman lineage, the objective of this investigation was to carry out a morpho-quantitative study of the myenteric neurons in the ileum, by means of histological sections and whole-mount muscular preparations treated by the NADH-diaphorase method. The profiles of the cell bodies (CB) of the neurons in the mesenteric and antimesenteric regions were counted and measured. The neurons were classified according to the dimensions of the CBs. NADH-dp myenteric neurons were observed grouped together into ganglia in the muscular tunica. The mean neuronal density was 985.8 ± 195.4 neurons/8.96 mm 2 in the antimesenteric region and 1267.8 ± 259.92 neurons/8.96 mm 2 in the mesenteric region. The incidences of small, medium and large neurons were 14.4, 82 and 3.6% in the antimesenteric region and 14.6, 70.8 and 14.4% in the mesenteric region, respectively. It was concluded that ganglionated arrangements and medium-sized NADH-dp neurons predominated in the myenteric plexus of adult Holtzman rats. The results observed indicated that the NADH-dp myenteric neurons of the ileum of Holtzman rats are similar to those of rats of Wistar lineage with respect to their localization, ganglionated arrangement and the predominance of neurons with medium-sized CBs.
Neurogastroenterology is defined as neurology of the gastrointestinal tract, liver, gallbladder and pancreas and encompasses control of digestion through the enteric nervous system (ENS), the central nervous system (CNS) and integrative centers in sympathetic ganglia. This Review provides a broad overview of the field of neurogastroenterology, with a focus on the roles of the ENS in the control of the musculature of the gastrointestinal tract and transmucosal fluid movement. Digestion is controlled through the integration of multiple signals from the ENS and CNS; neural signals also pass between distinct gut regions to coordinate digestive activity. Moreover, neural and endocrine control of digestion is closely coordinated. Interestingly, the extent to which the ENS or CNS controls digestion differs considerably along the digestive tract. The importance of the ENS is emphasized by the life-threatening effects of certain ENS neuropathies, including Hirschsprung disease and Chagas disease. Other ENS disorders, such as esophageal achalasia and gastroparesis, cause varying degrees of dysfunction. The neurons in enteric reflex pathways use a wide range of chemical messengers that signal through an even wider range of receptors. These receptors provide many actual and potential targets for modifying digestive function.
A histochemical technique was used to stain the myenteric neurons in the intact wall of the small intestine of mice, guinea-pigs and sheep. The length and diameter of the small intestine and the total serosal surface area were also obtained. Myenteric neurons were counted on large whole-mount preparations of the muscularis externa. Counts were carried out also on the submucosal plexus, on a more limited scale. In the mouse a spatial density of 10,600 myenteric neurons per cm2 was found. The small intestine was 33 cm long and measured on average 11.5 mm in circumference, the total outer surface (serosal surface) amounting to about 38.0 cm2. The total number of myenteric neurons in the small intestine was calculated as about 403,000. In the guinea-pig the length of the small intestine was 145 cm, the average circumference 22 mm and the total outer surface area about 319 cm2. The neuronal packing density was 8600/cm2, and the total number of myenteric neurons about 2,750,000. In the sheep the small intestine was about 2100 cm long with an average circumference of 60 mm and a total surface area of about 12,600 cm2. The ganglion neuron density was about 2500/cm2, and the total number of myenteric neurons in the small intestine was calculated as about 31,500,000. Thus, in the sheep the small intestine contained about 11 times as many myenteric neurons as the guinea-pig and about 80 times as many as the mouse. The differences are in the same direction as, but not proportional to, the differences in body weight and in the length of the intestine. The neuronal spatial density was highest in the mouse and lowest in the sheep, and in the sheep the neurons were markedly larger, and gathered in ganglia that were larger and further apart from one another, than in the mouse, while they had intermediate values in the guinea-pig. A new way of expressing neuronal packing densities is presented together with the proposal of an arbitrary but reproducible unit of intestinal length (a segment whose length is equal to its diameter). In the submucosal plexus the neuronal density was about 3000/cm2 in the guinea-pig, about 8700/cm2 in the mouse and about 4500/cm2 in the sheep. In the mouse the submucosal neuron density decreased gradually along the length of the small intestine.
The simple stomachs of Tadarida brasiliensis, Myotis velifer, and Antrozous pallidas are quite similar histologically, and contain gastric glands of the tubular variety seen in mammals generally. The stomach of Leptonycteris sanborni differs in being more saccular and in having tubular gastric glands that have few chief cells. The stomach of Desmodus rotundus was found to have an extremely long fundic or cardiac caecum, which contained acinar and tubuloacinar glands quite unlike gastric glands previously described in Mammalia.
The enteric nervous system is one of the three divisions of the autonomic nervous system, the others being the sympathetic and parasympathetic. In contrast to the other divisions, it can perform many functions independently of the central nervous system. It consists of ganglionated plexuses, their connections with each other, and nerve fibres which arise from the plexuses and supply the muscle, blood vessels and mucosa of the gastrointestinal tract. The enteric nervous system contains a large number of neurons, approximately 107 to 108. About ten or more distinct types of enteric neurons have been distinguished on electrical, pharmacological, histochemical, biochemical and ultrastructural grounds as well as on the basis of their modes of action. Both excitatory and inhibitory nerves supply the muscle and there are inhibitory and excitatory interneurons within the enteric plexuses. There are also enteric nerves which supply intestinal glands and blood vessels, but these receive less emphasis in this commentary.
Major advances have been made in our understanding of the nervous system in the gastrointestinal tract, the enteric nervous system. Because of its importance, neurogastroenterology is being increasingly recognised in clinical pharmacology. The enteric nervous system is a collection of neurones that can function more or less independently of the central nervous system and controls or modulates motility, exocrine and endocrine secretions, microcirculation and immune and inflammatory processes. Increasing knowledge of the physiology, pathophysiology, and pharmacology of the enteric nervous system will provide a basis for creation of new approaches to the treatment of gastrointestinal disorders. This review is part one of three and will describe the organisation and classification of the enteric nervous system.
The enteric nervous system (ENS) as the "brain of the gut" is pivotal for normal muscle activity in the gut. Neuronal circuits within the ENS are designed to control gut motility independent of central inputs. To fulfill this task the ENS contains all necessary elements for coding mechanical and chemical stimuli, interneuronal communication and efferent output to the muscle. This review provides a summary of the ENS circuits that control muscle activity, the main transmitters and neuromodulators involved and the functional implications for the normal and diseased gut.
The gastrointestinal (GI) tract is innervated by intrinsic enteric neurons and by extrinsic projections, including sympathetic and parasympathetic efferents as well as visceral afferents, all of which are compromised by age to different degrees. In the present review, we summarize and illustrate key structural changes in the aging innervation of the gut, and suggest a provisional list of the general patterns of aging of the GI innervation. For example, age-related neuronal losses occur in both the myenteric plexus and submucosal plexus of the intestines. These losses start in adulthood, increase over the rest of the life span, and are specific to cholinergic neurons. Parallel losses of enteric glia also occur. The extent of neuronal and glial loss varies along an oral-to-anal gradient, with the more distal GI tract being more severely affected. Additionally, with aging, dystrophic axonal swellings and markedly dilated varicosities progressively accumulate in the sympathetic, vagal, dorsal root, and enteric nitrergic innervation of the gut. These dramatic and consistent patterns of neuropathy that characterize the aging autonomic nervous system of the GI tract are candidate mechanisms for some of the age-related declines in function evidenced in the elderly.
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