Pre‐ovulatory temperature gradients within mammalian ovaries: a review

Abstract

Introductory perspectiveA long-standing problem in reproductive physiology concerns the temperature at which mammalian gonads function after the onset of puberty. In a majority of species so far studied, the testes descend via the inguinal canals to become suspended in a scrotal sac. Under normal conditions, a gradient in temperature is demonstrable between the abdomen and the scrotal pole of the testis (Setchell, 1978;Waites and Setchell, 1990). Cooling is important for successful spermatogenesis since this vital process fails in naturally occurring cryptorchids or in animals rendered cryptorchid by a surgical approach. Indeed, in such animals, there is a progressive destruction of the germinal epithelium (Griffiths, 1893;Glover, 1960). However, not all mammals employ a scrotal strategy. For example, elephants, various species of Hyrax and marine mammals retain their testes within the abdomen (Millar and Glover, 1973;Harrison, 1975;Glover et al., 1990), and a question therefore arises as to the temperature of such gonads. Do they function at deep body temperature without consequent morphological or genetic lesions in the sperm cells (e.g. mutations) or might there be subtle physiological mechanisms at play to cool such testicular tissue?Turning to the female, do mammalian ovaries function at deep body temperature or might there be compartments within ovarian tissues that are cooler than elsewhere in the gonad? It could be argued that if a reduction in temperature is required in the male gonad for successful gametogenesis, then temperature gradients would be anticipated within mammalian ovaries in tissues directly associated with the complement of oocytes -that is in follicular tissues.In fact, there are diverse reports of cooler tissues in the ovaries of various mammals (Balin et al., 1965;Benoit et al., 1976), and specifically in preovulatory Graafian follicles of rabbits and women. As determined by infra-red scanning (thermo-sensing) or by microelectrodes introduced during mid-ventral laparotomy, pre-ovulatory follicles of rabbits could be SummaryThe existence of a temperature gradient between the testis and deep body temperature has been accepted for many years. It is based on two simultaneous principles: cooling of the testis through the scrotal wall and transfer of heat between the testicular blood vessels. The ovary is positioned in the abdomen; a temperature difference parallel to the male system therefore seems less likely. However, the temperature of large follicles has been found to be 0.5 to 1.5°C cooler than the ovarian stroma in rabbits, pigs and, probably, women. The temperature difference seems to be based on a heat-consuming process in the expanding follicullar fluid, and a local transfer of heat between intra-ovarian blood vessels. The reason for the temperature gradient is not yet known; one may speculate of a common reason for the cooling of the gamete in male and female.

Counter-current transfer in reproductive biology

“…Grinsted et al (1980) found temperature gradients within different tissues of the rabbit ovary: large follicles were cooler than the ovarian stroma; the topic has been reviewed recently (Hunter 2003, Hunter & Einer-Jensen 2004. The temperature difference was confirmed in pigs, with measurements made during both laparotomy and laparoscopy (Hunter et al 2000).…”

‘There is only one thing that is truly important in an IVF laboratory: everything’ Cairo Consensus Guidelines on IVF Culture Conditions

“…Similarly, the temperature of the female reproductive tract might also be lower than core body temperature: a temperature gradient exists in the oviduct of pigs and rabbits, with the isthmus being 0.2-1.6°C cooler than the ampulla (Hunter, 2012;Hunter and Nichol, 1986;Hunter et al, 2006). Mature follicles in rabbit, pigs and cows are 1.3-1.7°C cooler than the ovarian stroma (Grinsted et al, 1980;Hunter, 2012;Hunter and Einer-Jensen, 2005;Hunter et al, 1997Hunter et al, , 2000Hunter et al, , 2006 and ∼2.3°C cooler than stroma in human ovaries (Grinsted et al, 1985). Such observations, as well as a lack of reliable information on the uterine temperature at the time of implantation, have led to the proposition that human embryo development might benefit from a temperature lower than core body temperature (Leese et al, 2008).…”

Sperm transport and retention at the fertilization site is orchestrated by a chemical guidance and oviduct movement

“…Instead, thermotaxis may have a different role under in vivo conditions, for example, guiding capacitated spermatozoa along the cumulus matrix. Hyaluronic acid (the main component of the cumulus matrix) is a highly hygroscopic molecule, which preferentially binds water molecules, decreasing local temperature (Hunter & Einer-Jensen 2005). Thus, the gradual distribution of hyaluronic acid (higher concentration in the periphery of the cumulus) could facilitate an increasing temperature gradient toward the oocyte vicinity.…”