Abstract
The postnatal development of neuropeptide Y- and calcitonin gene-related peptide-immunoreactive (NPY-IR and CGRP-IR) nerve fibers in the rat urinary bladder was investigated using whole-mount preparations and cryostat sections. In newborn and 3-day-old rats, many NPY-IR nerve fibers were observed in the subserous and muscle layers. Many NPY-IR nerve cell bodies clustered at branching points of the subserous nerve bundles. Within 4 weeks after birth, these cell bodies drastically decreased in number and spread along the bundles, although the number of NPY-IR nerve fibers increased moderately. In contrast, CGRP-IR nerve fibers in newborn and 3-day-old rats were less developed, and no CGRP-IR nerve cell body was observed in any rat. However, CGRP-IR nerve fiber distribution in the urinary tissues conspicuously increased within 4 weeks after birth. Especially, an increase of the infraepithelial fibers showing a meshwork appearance was prominent in the fundus and corpus of the bladder. The infra- and intraepithelial CGRP-IR nerve meshwork of the ventral wall was more dense than that of the trigone. At 4 weeks, NPY-IR and CGRP-IR nerves were similar to those of the adult rat (8–12 weeks old). The present study suggests a correlation between the development of the peripheral nervous system in the urinary bladder and maturation of micturition behavior in the rat.
Similar content being viewed by others
References
Alm P, Elmér M (1975) Adrenergic and cholinergic innervation of the rat urinary bladder. Acta Physiol Scand 94:36–45
Alm P, Alumets J, Brodin E, Håkanson R, Nilsson G, Sjöberg NO, Sundler F (1978) Peptidergic (substance P) nerves in the genito-urinary tract. Neuroscience 3:419–425
Alm P, Alumets J, Håkanson R, Owman C, Sjöberg NO, Stjernqvist M, Sundler F (1981) Enkephalin-immunoreactive nerve fibers in the feline genito-urinary tract. Histochemistry 72:351–355
Buckley TL, Brain SD, Rampart M, Williams TJ (1991) Time-dependent synergistic interaction between the vasodilator neuropeptide, calcitonin gene-related peptide (CGRP) and mediators of inflammation. Br J Pharmacol 103:1515–1519
Capek K, Jelinek J (1956) The development of the control of water metabolism. I. The excretion of urine in young rats. Physiol Bohemoslov V: 91–96
De Groat WC, Douglas JW, Glass J, Simonds W, Weimer B, Werner P (1975) Changes in somato-vesical reflexes during postnatal development in the kitten. Brain Res 94:150–154
El Badawi A (1987) Comparative neuromorphology in animals. In: Torrens M, Morrison JFB (eds) The physiology of the lower urinary tract. Springer, Berlin Heidelberg New York, pp 23–51
El Badawi A, Schenk EA (1966) Dual innervation of the mammalian urinary bladder: a histochemical study of the distribution of cholinergic and adrenergic nerves. Am J Anat 119:405–428
Fuller RW, Conradson TB, Dixon CMS, Crossman DC, Barnes PJ (1987) Sensory neuropeptide effects in human skin. Br J Pharmacol 92:781–788
Gosling JA, Dixon JS (1974) Sensory nerves in the mammalian urinary tract: an evaluation using light and electron microscopy. J Anat 117:133–144
Gosling JA, Dixon JS (1975) The structure and innervation of smooth muscle in the wall of the bladder neck and proximal urethra. Br J Urol 47:549–558
Gu J, Polak JM, Blank MA, Terenghi G, Morrison JFB, Bloom SR (1984) The origin of VIP-containing nerves in the urinary bladder of rat. Peptides 5:219–223
Holzer P (1988) Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience 24:739–768
Hsu SM, Raine L, Fanger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 4:577–580
Iravani MM, Zar MA (1988) Evidence for neuropeptide Y (NPY) as the probable non-cholinergic motor transmitter in rat urinary bladder in vitro. J Physiol (Lond) 403:61
Kruse MN, De Groat WC (1990) Micturition reflexes in decerebrate and spinalized neonatal rats. Am J Physiol 258:R1508-R1511
Kuma Y (1979) The autonomie innervation in experimental neurogenic bladder of the rat (in Japanese). Nippon Hinyokika Gakkai Zasshi 70:1366–1378
Kuru M (1965) Nervous control of micturition. Physiol Rev 45:425–494
Lundberg JM, Terenius L, Hökfelt T, Martling CR, Tatemoto K, Mutt V, Polak J, Bloom S, Goldstein M (1982) Neuropeptide Y (NPY)-like immunoreactivity in peripheral noradrenergic neurons and effects of NPY on sympathetic function. Acta Physiol Scand 116:477–480
Maggi CA, Santicioli P, Meli A (1984) Postnatal development of myogenic contractile activity and excitatory innervation of rat urinary bladder. Am J Physiol 247: R972-R978
Maggi CA, Santicioli P, Meli A (1986) Postnatal development of micturition reflex in rats. Am J Physiol 250:R926-R931
Maggi CA, Santicioli P, Geppetti P, Frilli S, Spillantini MG, Nediani C, Hunt SP, Meli A (1988) Biochemical anatomical and functional correlates of postnatal development of the capsaicin-sensitive innervation of the rat urinary bladder. Dev Brain Res 43:183–190
Malmgren A, Ekblad E, Sundler F, Andersson K-E, Andersson PO (1990) Muscarinic supersensitivity in the rat urinary bladder after capsaicin pretreatment. Acta Physiol Scand 138:377–387
Mattiasson A, Ekblad E, Sundler F, Uvelius B (1985) Origin and distribution of neuropeptide Y-, vasoactive intestinal polypeptide and substance P-containing nerve fibers in the urinary bladder of the rat. Cell Tissue Res 239:141–146
McNeill DL, Harris CH, Holzbeierlein JM, Shew RL, Traugh NE, Papka RE (1992) CGRP-immunoreactive primary afferent nerve fibers in the rat urinary bladder: effects of dorsal rhizotomy and MK-801. Exp Neurol 118:317–323
Morrison JFB (1987) Bladder control: role of higher levels of the central nervous system. In: Torrens M, Morrison JFB (eds) The physiology of the lower urinary tract. Springer, Berlin Heidelberg New York, pp 237–274
Noden DM, Lahunta DA (1985) Derivatives of the intermediate mesoderm: urinary system, adrenal gland. In: Stamathis G (ed) The embryology of domestic animals: developmental mechanisms and malformations. Williams & Wilkins, Baltimore, pp 312–321
Pittam BS, Burnstock G, Purves RD (1987) Urinary bladder intramural neurones: an electrophysiological study utilizing a tissue culture preparation. Brain Res 403:267–278
Rosenfeld MG, Mermod JJ, Amara SG, Swanson LW, Sawchenko PE, Rivier J, Vale WW, Evans RM (1983) Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing. Nature 304:129–135
Santicioli P, Maggi CA, Meli A (1985) The effect of capsaicin pretreatment on the cystometrograms of urethane-anesthetized rats. J Urol 133:700–703
Sharkey KA, Williams RG, Schultzberg M, Dockray GJ (1983) Sensory substance P-innervation of the urinary bladder: possible site of action of capsaicin in causing urinary retention in rats. Neuroscience 10:861–868
Stelzner DJ (1971) The normal postnatal development of synaptic end-feet in the lumbosacral spinal cord and responses in the hind limbs of the albino rat. Exp Neurol 31:337–357
Tohyama M, Shiotani Y (1986) Neuropeptides in spinal cord. Prog Brain Res 66:177–218
Weihe E (1990) Neuropeptides in primary afferent neurons. In: Zenker W, Neuhuber WL (eds) The primary afferent neurons. A survey of recent morpho-functional aspects. Plenum Press, New York, pp 127–159
Weihe E, Hartschuh W, Reinecke M (1983) Multilocal distribution of neural substance P in the skin of man and other mammals: immunohistochemical evidence for complex interaction with multitarget neurotensinergic and VIP-ergic nerves. In: Skrabanek P, Powell D (eds) Substance P — Dublin 1983. Boole Press, Dublin, pp 143–144
Yamada M (1984) Innervation of the rat urinary bladder. II. Effects of prostaglandins on the denervated detrusor muscle after bilateral pelvic ganglionectomy (in Japanese). Nippon Heikatsukin Gakkai Zasshi 20:483–491
Yokokawa K, Sakanaka M, Shiosaka S, Tohyama M, Shiotani Y, Sonoda T (1985) Three-dimensional distribution of substance P-like immunoreactivity in the urinary bladder of rat. J Neural Transm 63:209–222
Yokokawa K, Tohyama M, Shiosaka S, Shiotani Y, Sonoda T, Emson PC, Hillyard CV, Girgis S, MacIntyre I (1986) Distribution of calcitonin gene-related peptide-containing fibers in the urinary bladder of the rat and their origin. Cell Tissue Res 244:271–278
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Iuchi, H., Satoh, Y. & Ono, K. Postnatal development of neuropeptide Y- and calcitonin gene-related peptide-immunoreactive nerves in the rat urinary bladder. Anat Embryol 189, 361–373 (1994). https://doi.org/10.1007/BF00190591
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00190591