Set in an historical perspective, this essay examines diverse physiological aspects of Fallopian tube function in domestic animals and man. Microsurgical experiments are described that established the role of the isthmus in imposing a sperm gradient up to the site of fertilisation. Resection of the isthmus followed by reanastomosis of the remaining portions of the tube generated a high incidence of polyspermy in mated animals. Scanning electron microscopy and surgical studies revealed that spermatozoa were arrested and stored in the caudal portion of the isthmus before ovulation, the so-called functional sperm reservoir. There were specific adhesion contacts between the sperm head and endosalpingeal microvilli or cilia. Further experiments indicated that very large numbers of competent spermatozoa could be released from pre-ovulatory binding by microinjections of a solution of progesterone in oil under the serosal layer of the tube: when suitably timed, such treatment led to a high incidence of polyspermic fertilisation. Avid sperm binding in the caudal isthmus before ovulation prevents myosalpingeal activity leading to abnormal fertilisation, as might occur with multiple mating. Temperatures in the reproductive system were assessed and the caudal isthmus was found to be cooler than the ampulla during the pre-ovulatory phase of sperm storage. Finally, the existence of fluid microenvironments within the Fallopian tubes was reported, and the role of suspended cumulus-corona cells in amplifying signals from the zygote examined. An impact of Fallopian tube fluids on embryonic gene expression was also considered--an influence that may be further imposed if such fluids have access to the uterine lumen.

This essay argues strongly that for those sperm cells involved in fertilisation, the process of capacitation represents an active and specific coordination within succeeding regions of the female tract and one whose completion is synchronised with the events of ovulation. Observations on the time‐course of capacitation when spermatozoa are first exposed to the uterus and then progress to the Fallopian tubes indicate a synergistic influence of these adjoining portions of the female tract on the rate of capacitation. Three concepts on the control of capacitation are introduced to emphasise the importance of integration in vivo, namely that (1) completion of capacitation is a peri‐ovulatory event, (2) suppression of completion of capacitation is an essential storage strategy during a long pre‐ovulatory interval, and (3) the process of capacitation comes under the influence of local and systemic ovarian control mechanisms, especially the secretion of progesterone from Graafian follicles soon to ovulate. The last would act to coordinate the final maturation and meeting of male and female gametes. Despite the preceding points, the requirement for such integrated in vivo programming of sperm cell maturation can clearly be overridden in systems of culture. The most reasonable interpretation here would be that a microdrop of culture medium containing eggs, follicular cells and components of follicular fluid would to a considerable extent represent a post‐ovulatory environment. Within such a preparation, there would be leaching of the sperm surface among the relatively vast and heterogeneous population of cells, and a proportion of spermatozoa could then respond to ‘post‐ovulatory signals’, not least to molecular influences of the zona pellucida and vitelline products for completion of capacitation. Nonetheless, a physiologically meaningful interpretation of capacitation calls for a stepwise analysis of the dynamic interactions between sperm cell and female tract at successive stages between the uterus and ampullary‐isthmic junction. Mol. Reprod. Dev. 67:243–250, 2004. © 2004 Wiley‐Liss, Inc.

This paper is concerned with endosalpingeal specialisations that underlie stabilisation of unique secretions forming microenvironments within the Fallopian tube lumen, not least as they influence the final stages of sperm transport and maturation. In particular, a specific microenvironment at the ampullary-isthmic junction in the presence of the newly-shed oocyte(s), associated granulosa cells and their secretory products is thought to characterise the site of fertilisation. Attention is also drawn to the viscous glycoprotein in the caudal isthmus before ovulation: it isolates spermatozoa stored with suppressed motility from the metabolic stimulation caused by uterine or ampullary fluid. This viscous secretion strips male antigens from the sperm surface, facilitating their preovulatory binding reactions to organelles of the isthmus epithelium. Peri-ovulatory activation of discrete numbers of viable spermatozoa is regulated by follicular progesterone secretion, but seemingly involves local mobilisation of Ca2+ ions into bound gametes of appropriate membranous maturity. Motility and progression to the site of fertilisation may be further heightened by an influence of catecholamines diffusing from the myosalpinx; receptors for such molecules are present on the sperm surface. There is tight control of sperm activation and release close to the time of ovulation, generating initial sperm:egg ratios at the ampullar-isthmic junction of close to unity. However, with establishment of the block to polyspermy in newly activated eggs and lapse of time after ovulation, control of sperm progression soon relaxes. Indeed, 2-4 cell embryos may contain large numbers of accessory spermatozoa on or in the zona pellucida.

Mares were inseminated with motile spermatozoa suspended in 30-150 microliters Tyrode's medium directly onto the uterotubal papilla at the anterior tip of the uterine horn, ipsilateral to the ovary containing a dominant preovulatory follicle of > or = 35 mm in diameter, by means of a fine gamete intrafallopian transfer (GIFT) catheter passed through the working channel of a strobed light videoendoscope. Insemination of 10, 8, 25, 14, 11 and 10 mares with, respectively, 10.0, 5.0, 1.0, 0.5, 0.1 or 0.001 x 10(6) motile spermatozoa resulted in conception rates of, respectively, 60, 75, 64, 29, 22 and 10%. Deposition of 1.0 x 10(6) motile spermatozoa onto the uterotubal papilla began to approach the limit of successful fertilization. These doses are far lower than the 3-15 x 10(9) spermatozoa normally ejaculated by fertile stallions during mating, and the accepted minimum dose of 500 x 10(6) spermatozoa used for conventional uterine body insemination in mares. The simplicity of the technique offers a practical means of exploiting new breeding technologies that require very small numbers of spermatozoa in horse breeding.

After describing the site of fertilisation and that of the functional sperm reservoir in the female tract, proposals are made concerning a modified site of sperm deposition. A deep pre-ovulatory insemination into the ipsilateral uterine horn - the side adjoining the ovulatory follicle - should raise the chances of establishing viable spermatozoa in the isthmus where they would undergo storage, Suppressed morility within viscous secretions and binding of the head to endosalpingeal microvilli characterise this phase, Release and activation of such spermatozoa would be prompted by imminent ovulation and associated endocrine programming delivered via a local route.Potential advantages of deep insemination include (I) raising the overall fertility of genetically valuable bulls whose non-return rates are sub-optimal; (2) reducing the number of spermatozoa in each insemination dose; (3) using effectively the limited numbers of sex-selected sperm cells (X and Y chromosome bearing, spermatozoa), currently available from flow cytometry; and (4) breeding from valuable but oligospermic bulls, Putative disadvantages might include (1) rectal palpation of the ovaries to locate the preovulatory follicle; (2) damage or even perforation of the uterine wall by the;deep insemination catheter; (3)risk of polyspermic fertilisation; and (4) the inappropriateness of the technique for non-clinically qualified inseminators. Each of these reservations is responded to in a rational manner. In conclusion, a modified technique of insemination would be feasible under commercial conditions, might enable retention of genetically valuable bulls deemed of only average fertility under test conditions, and could give a welcome boost to a sagging artificial insemination industry.

Nichol et al (1992, Journal of Reproduction and Fertility, 96, 699–707) identified a pre- to post-ovulatory decrease (approx 1mM) in the amount of glucose in pig oviduct fluid. The present studies investigated whether the decrease was due to metabolism by embroyos and/or oviduct tissues, and also whether there was a local influence of the ovary on the oviduct fluid content of energy substrates. Unilaterally ovariectomised pigs were used, in which, through compensation, oviducts that contained twice the normal number of embryos could be compared with oviducts which contained no embryos. Following unilateral ovariectomy and after two oestrous cycles of normal duration, surgery was performed 88 hours after the beginning of standing heat to obtain oviduct fluid samples, just before embryonic entry into the uterus. Luminal fluid samples from the ampulla and ampullary-isthmic junction from oviducts with and without an adjacent ovary were assayed for glucose, pyruvate and lactate concentrations. No significant differences were found between the glucose, pyruvate and lactate concentrations in fluids from the ampulla or ampullaryisthmic junction from oviducts containing embryos compared with absence of embryos (P > 0·05). Therefore, the post-ovulatory decrease was not due to the presence of embryos or to a local effect of the ipsilateral ovary. Consequently, pig oviduct fluid concentrations of glucose, lactate and pyruvate are seemingly regulated by systemic mechanisms.

Diverse lines of evidence suggest that the Fallopian tubes make no overwhelming contribution to human reproduction other than as a conduit for gametes and embryos. Even so, bearing in mind global success rates for in vitro fertilization (IVF) coupled with uterine transplantation of embryos (20% fruitful pregnancies), the Fallopian tubes may make a subtle contribution to reproductive performance. The experimental evidence from monkeys and man arguing against an essential rôle for the tubes -- at least in individual instances -- would include (1) the results of Estes' operation, when ovaries are autotransplanted into the uterine lumen in women with blocked or missing Fallopian tubes and pregnancy ensues; (2) asynchronous embryo transfer when newly fertilized (pronucleate) eggs transplanted to the uterus can generate a pregnancy; (3) the transcervical transfer after IVF of early cleavage stage human embryos into the uterus, with subsequent establishment of pregnancy; (4) the trans-cervical transfer of human spermatozoa and oocytes into the uterus to give pregnancy, indicating that capacitation, fertilization and the earliest stages of embryonic development can be achieved in the uterus. In endeavoring to explain contrasts between these successful procedures in primates and their failure in non-primates, perhaps the simplex uterus in primates compared with a bicornuate or bipartite uterus in laboratory and farm species has relevance: there is lack of a clear-cut distinction between the endometrium and endosalpinx in the intra-mural segment and potential mixing of uterine and tubal fluids. Indeed, the latter may explain in part a susceptibility to tubal ectopic pregnancy, coupled with proliferating endometrial fragments in the Fallopian tube.

After discussing the rate of functional sperm transport to the Fallopian tubes of sheep, cows and pigs, this review focuses on the relatively protracted preovulatory storage of spermatozoa in the caudal portion of the isthmus, with suppressed motility and sperm head adhesion to the epithelium. As well as facilitating the phase of sperm storage, the viscous secretions in this region of the duct may serve to pre vent access of uterine and ampullary fluids into the isthmus sperm reservoir, and similarly entry of a uterine population of polymorphonuclear leucocytes. Ovarian endocrine control of peri-ovulatory sperm activation and release is analysed, with emphasis on a local counter-current vascular exchange of relatively high concentrations of follicular hormones to programme the isthmus and its content of male gametes. The site and time of completion of capacitation are reviewed critically, as are these aspects of hyperactivation and the acrosome reaction. The specific fluid milieu of the ampullary-isthmic junction in the presence of egg investments may be closely involved in triggering these final events for a fertilising spermatozoon, but it is strongly argued also that pre-ovulatory suppression of completion of capacitation is an essential storage strategy. The extremely low initial sperm:egg ratios are considered in terms of (1) molecular modulation of sperm numbers activated from the isthmus sperm reservoir and (2) molecular signals within the cumulus oophorus aggregates of polytocous species. A potential influence of temperature gradients within the Fallopian tubes in guiding viable spermatozoa towards the site of fertilisation is examined, and the post-ovulatory increase in sperm numbers reaching the ampulla after establishment of an il) eversible block to polyspermy is emphasised.

The pH of the oviduct lumen was measured at different stages of the estrous cycle in the ampulla and ampullary-isthmic junction (AIJ) of intact and unilaterally ovariectomized mated or nonmated pigs. The pH profile consisted of high frequency small peaks superimposed on low frequency large amplitude peaks. One animal examined at midcycle exhibited fluctuations in pH (peak to nadir; delta pH) of 0.3 and 0.7 units in the ampulla and AIJ, respectively, and the frequencies of the large peaks in these regions were 2.6 and 1.6 peaks.min-1, respectively. In six preovulatory unmated pigs, the delta pH (mean +/- SE) was 0.50 +/- 0.04 units in both regions and the large peak frequencies were 0.6 +/- 0.06 peaks.min-1. In one animal that was assessed during ovulation, the pH showed deviations of up to 0.4 pH units, which were probably due to the alkalinity of follicular fluid accompanying the ovulated eggs. In the ampullae of five unilaterally ovariectomized postovulatory-mated pigs, the delta pH in oviducts with and without an ipsilateral ovary was significantly lower than preovulatory (p < 0.05), but the large and the small peak frequencies were not significantly different. By contrast, the delta pH in the AIJ with an ipsilateral ovary (0.11 +/- 0.02 units) was significantly lower than before ovulation (0.54 +/- 0.04 units) and also when compared with the contralateral AIJ (0.36 +/- 0.06 units) (p < 0.05). The ovary also influenced the small peak frequency, which was significantly higher if the ipsilateral ovary was absent (10.7 +/- 1.5 vs. 14.9 +/- 1.6 peaks.min-1, respectively). Thus, oviduct fluid pH is controlled by both systemic and local mechanisms, and the ipsilateral ovary and (or) embryonic factors influence the pH profile of the oviduct.

Hydrosalpinges were created to collect adequate volumes of fluid during pre-, peri- and postovulatory intervals from the ampulla, ampullary-isthmic junction and the isthmic-utero-tubal junction of the oviducts from Large White gilts that had exhibited at least two natural oestrous cycles. The accumulated fluids, follicular fluid and Butschwiler's medium were compared for their effects on various parameters of boar sperm motility using the CellSoft, computer-assisted, digital image analysis system. Sperm velocity (micron s-1 +/- SEM) was significantly higher (P < 0.05) in follicular fluid (84 +/- 3; n = 5) than in fluids from the ampulla during peri- and early postovulatory intervals, and from the isthmic-utero-tubal junction during pre- and early postovulatory intervals. It was also higher (P < 0.05) than in the fluid from the ampullary-isthmic junction during pre- and early postovulatory intervals; however, sperm velocity in follicular fluid was not significantly different from that in the periovulatory fluid from the ampullary-isthmic junction. The mean lateral head displacement (ALHmean) of spermatozoa was significantly greater in follicular fluid (3.9 +/- 0.3 microns; n = 5) than in fluid from the ampulla during peri- and early postovulatory intervals and from the isthmic-utero-tubal junction during pre- and early postovulatory intervals, and was also higher (P < 0.05) than in fluid from the ampullary-isthmic junction during the preovulatory period, but was not different from the peri- and postovulatory ampullary-isthmic junction fluids. The proportion of spermatozoa exhibiting circular motion was significantly higher (P < 0.05) in the periovulatory fluid from the ampullary-isthmic junction (24 +/- 3%) compared with fluids obtained during preovulatory and early postovulatory periods. Follicular fluid had no effect on the proportion of spermatozoa exhibiting circular motion. The average radius of sperm movement in circular trajectories was higher in follicular fluid than in the periovulatory fluids from the ampulla and ampullary-isthmic junction (P < 0.05). In hydrosalpingeal fluids collected 2-5 days after ovulation, the average radius of movement was greater in the ampulla fluid and ampullary-isthmic junction fluid than in fluid from the isthmic-utero-tubal junction (P < 0.05). These results demonstrate that follicular fluid and oviductal fluids have considerable influences on boar sperm motility. Furthermore, the immediate effect of periovulatory ampullary-isthmic junction fluid in increasing the percentage of spermatozoa swimming in circles (hyperactivated) is relevant, since it is at this time and within this region that fertilization occurs.

Reproduction in Domestic AnimalsVolume 31, Issue 1 p. 51-55 HOW, WHEN and WHERE DO SPERMATOZOA GAIN THEIR FERTILISING ABILITY IN VIVO? R.H.F. Hunter, R.H.F. Hunter University of Edinburgh, Edinburgh, ScotlandSearch for more papers by this author R.H.F. Hunter, R.H.F. Hunter University of Edinburgh, Edinburgh, ScotlandSearch for more papers by this author First published: August 1995 https://doi.org/10.1111/j.1439-0531.1995.tb00005.xCitations: 10AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Citing Literature Volume31, Issue1August 1995Pages 51-55 RelatedInformation

This essay considers the means whereby sperm/egg ratios close to unity are generated during the initial stages of fertilisation in placental mammals. Pre-ovulatory graafian follicles and their contents are seen to be key structures orchestrating the events of sperm progression and coordinating the subsequent meeting of male and female gametes. Three levels of control over the numbers of spermatozoa activated and released from the functional reservoir in the caudal region of the fallopian tube isthmus are proposed. A primary control would be obtained by means of a countercurrent transfer of ovarian follicular progesterone from the ovarian vein into the tubal branch of the ovarian artery. The concentration of progesterone so transferred would be proportional to the number of preovulatory follicles, and thus to the number of eggs to be shed, and would act progressively to reduce sperm binding to the endosalpinx of the caudal isthmus. Differential timing of the release from epithelial binding may be a crucial means of achieving the initial low sperm/egg ratios. A secondary regulation of the release of graded numbers of viable spermatozoa towards the ampullary-isthmic junction of the fallopian tubes would be by means of molecular messages derived from the mucified oocyte-cumulus complex shortly before and after the time of ovulation. Third would be reorientation of sperm trajectories by molecular gradients within the cumulus cell mass to direct competent spermatozoa to those oocytes as yet unpenetrated. Together these differing levels of control would impose low sperm/egg ratios during the initial stages of fertilisation, such strict quantitative regulation of male gametes lasting at least until the block to polyspermy is fully established and the vitellus is no longer at risk from further sperm penetration. (C) 1996 Wiley-Liss, Inc.

This review considers the problem of ovotestis formation in animals of 38,XX chromosome complement. After a clinical description, attention focuses on the condition of the gonads and genital tract. A complete spectrum of gonadal types has been found, ranging from a single ovotestis almost invariably on the right-hand side to both gonads appearing as testicular-like structures, sometimes with a distinct tunica albuginea. The ovotestis or testis-like structure may have descended to an inguinal or scrotal location. Although interstitial cells of Leydig and seminiferous tubules were always abundant in testicular tissue, germ cells were never present. The lumen of the seminiferous tubules was packed with pale-staining, Sertoli-like cells. A bicornuate uterus was characteristic but suppression of the proximal portion of the Müllerian duct always adjoined an ovotestis; a corresponding development of the Wolffian duct featured as a convoluted epididymis. Inhibition of the Fallopian tube was attributed to a local influence of AMH from the Sertoli cells, as was the failure of small Graafian follicles within an ovotestis to respond to injected gonadotrophins. As to the aetiology of an ovotestis, defective colonisation of the genital ridges by primordial germ cells is considered, as is evidence for incorporation of adrenal cells into the embryonic gonad. Molecular probing has failed to reveal the classical sex-determining gene, Sry, and other Y-related DNA sequences such as Zfy and DYZI in almost all the intersex animals examined. Currently favoured as an explanation for ovotestis formation is a mutation in the inhibin gene within granulosa cells of Graafian follicles. Such a mutation would prompt secretion of the closely comparable glycoprotein molecule AMH in these genetic females, with a resultant progressive virilisation of gonadal tissue. The proposed mutation may be carried as an autosomal recessive gene by certain boars. Varying amounts of AMH secretion or differing timescales for the transition from inhibin to AMH could in part explain differing degrees of ovotestis formation. Despite this proposition, interactions between genes that prescribe functional testicular tissue, enhanced rates of gonadal development, and left-right asymmetries between the paired gonads now require systematic study.

Acta Obstetricia et Gynecologica ScandinavicaVolume 74, Issue 9 p. 677-681 Human sperm reservoirs and Fallopian tube function: a role for the intra-mural portion? Ronald H.F. Hunter, Ronald H.F. Hunter Faculty of Science, University of Edinburgh, Scotland, UKSearch for more papers by this author Ronald H.F. Hunter, Ronald H.F. Hunter Faculty of Science, University of Edinburgh, Scotland, UKSearch for more papers by this author First published: September 1995 https://doi.org/10.3109/00016349509021173Citations: 10 †32, Gilmour Road Edinburgh, EH16 5NT, Scotland, UK AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat References Hunter R HF. The Fallopian tubes; their role in fertility and infertility. Springer-Verlag, Berlin, Heidelberg 1988. Hunter R HF. Ovarian programming of gamete progression and maturation in the female genital tract. Zool J of Linnean Soc 1989; 95: 117–24. Hunter R HF. Physiology of the Fallopian tubes, with special reference to gametes, embryos and micro-environments. Proceedings of 7th Reinier de Graaf Symposium entitled From ovulation to implantation. Excerpta Medica, 1990; 101–19, Internal Congress Series, No 917. Hunter R HF. Behaviour of spermatozoa in the oviduct of farm animals. In: Proceedings of International Symposium on the Biology of the Oviduct. Arch Biol Med Exp 1991; 24: 349–59. Barratt C LR, Cooke ID. Sperm transport in the human female reproductive tract-a dynamic interaction. Int J Androl 1991; 14: 394–411. Drobnis EZ, Overstreet JW. Natural history of mammalian spermatozoa in the female reproductive tract. Oxford Reviews of Reproductive Biology 1992; 14: 1–45. Bedford JM. The contraceptive potential of fertilisation: a physiological perspective. Hum Reprod 1994; 9: 842–58. Croxatto HB. Gamete transport. Reproductive endocrinology, surgery and technology, EY Adashi, JA Rock, Z. 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The timing of capacitation in mammalian spermatozoa-a reinterpretation. Res Reprod 1987a; 19: 3–4. Hunter R HF. Human fertilisation in vivo, with special reference to progression, storage and release of competent spermatozoa. Hum Reprod 1987b; 2: 329–32. Williams M., Hill CJ, Scudamore I., Dunphy B., Cooke ID, Barratt C LR. Sperm numbers and distribution within the human Fallopian tube around ovulation. Hum Reprod 1993; 8: 2019–26. Edwards RG. Conception in the human female. Academic Press, London 1980. Hunter R HF. Ovarian regulation of sperm progression in the Fallopian tubes. Zygote 1994; 2: 363–6. Mortimer D.. Behaviour of spermatozoa in the human oviduct. Arch Biol Med Exp 1991; 24: 339–48. Citing Literature Volume74, Issue9September 1995Pages 677-681 ReferencesRelatedInformation