Effects of Complete Hypothalamic Deafferentation on the Estrous Phase of Follicle-Stimulating Hormone Release in the Cyclic Rat
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1 BIOLOGY OF RPRODUCTION 26, (1982) ffects of Complete Hypothalamic Deafferentation on the strous Phase of Follicle-Stimulating Hormone Release in the Cyclic Rat MICHAL. RUSH,2 OLADAPO A. ASHIRU3 and CHARLS A. BLAK4 Department of Anatomy University of Nebraska Medical Center Omaha, Nebraska ABSTRACT We investigated whether neural afferents to the medial basal hypothalamus play an acute role in the estrous phase of FSH release in the 4-day cyclic rat. A cannula was inserted into the right atrium of the heart under brief ether anesthesia during the early afternoon of proestrus for subsequent blood collections and injection of LHRH. In some of the rats, the medial basal hypothalamus was surgically isolated from the rest of the brain with a small knife under brief ether anesthesia between 2000 h and 2130 h of proestrus. Control groups consisted of naive rats which were not treated during the night of proestrus and sham-operated animals in which the knife was lowered to the corpus callosum between 2000 h and 2130 h of proestrus. Rats were bled at 2200 h of proestrus and at 0200 h, 0600 h and 1000 h of estrus for radioimmunoassay of plasma FSH and LH. The plasma FSH levels in all 3 groups between 2200 h of proestrus and 1000 h of estrus were elevated above levels observed in other cannulated rats bled prior to the onset of the proestrous phase of FSH release at h of proestrus. There were no statistically significant differences in plasma FSH or LII concentrations at any of the time periods between the 3 groups of serially bled rats. The deafferentation procedure did not appear to impair the pituitary gland s ability to secrete gonadotropins as injection of 50 ng of LHRH alter the bleeding at 1000 h of estrus caused substantial elevations in plasma FSH and LH concentrations which were not different between the 3 groups. The results suggest that neural afferents to the medial basal hypothalamus play no acute role in the estrous phase of FSH release in the cyclic rat. INTRODUCTION In the cyclic rat and hamster, folliclestimulating hormone (FSH) and luteinizing hormone (LH) concentrations rise in the plasma during the afternoon or proestrus. While plasma LII levels fall to approach presurge concentrations during the evening of proestrus, plasma FSH levels either remain elevated through mid-estrus or fall and rise again during the evening of proestrus to remain elevated through mid-estrus (Daane and Parlow, 1971; Butcher et al., 1974; Smith et a!., 1975; Siegel et a!., and Accepted November 17, Received August 31, Supported by grants from the NIH (HD11O11 HDO7097). 2Present address: Dept. of Anatomy, University of Kentucky Medical Center, Lexington, KY Present address: Dept. of Anatomy, University of Lagos, College of Medicine, Lagos, Nigeria, 4Correspondence: Dr. Charles A. Blake, Dept. of Anatomy, University of Nebraska Medical Center, Omaha, N ; Ashiru and Blake, 1978; lias and Blake, 1981). There may be species differences between rats and hamsters with respect to the neural mechanisms governing periovulatory FSH release. Whereas administration of phenobarbital during the early afternoon of proestrus blocks both the proestrous and estrous phases of FSH release in the rat (Ashiru and Blake, 1978), similar treatment in the hamster blocks only the proestrous phase of FSH release (Siege! et a!., 1976; Chappe! et a!., 1979). In the rat, both phases of FSH release appear to be dependent on a single neural signal entering the medial basal hypothalamus (MBH) from an anterior direction during the afternoon of proestrus which causes LH releasing hormone (LHRH) release (Ashiru and Blake, 1978; Rush et a!., 1980; Blake and Kelch, 1981; Hasegawa et a!., 1981). In the hamster, there may be 2 neural signals which enter the MBH from an anterior direction to cause the 2 phases of FSH release. It has been suggested that 1 signal activates LHRH release during the afternoon of proestrus to 399
2 400 RUSH T AL. cause the proestrous phase of FSH release and that a second, more prolonged, signal enters the MBH from an anterior direction during the afternoon and early evening of proestrus to cause the estrous phase of FSH release (Chappel et a!., 1979). Deafferentation and lesioning studies in the hamster suggest that the estrous phase of FSH release does not involve the immediate presence of neural afferents to the MBH but that it does require that the hypothalamic arcuate nuclei remain intact during the estrous phase of FSH release (Chappel et al., 1977). In the rat, anterior afferents to the MBH and LHRH play no acute role in the estrous phase of FSH release (Rush et a!., 1980; Hasegawa et a!., 1981; Blake and Kelch, 1981), and indirect evidence suggests that the brain may not play an acute role in the estrous phase of FSH release (lias and Blake, 1981). However, these studies in the rat do not completely rule out the possible involvement of an hypothalamic factor distinct from LHRH with a preferential FSH releasing ability. This factor could be released by neural input to the MBH from directions other than anterior during the late evening of proestrus and the morning of estrus. For example, noradrenergic neurons enter the MBH primarily from a lateral direction (Weiner et al., 1972), and it is possible that noradrenalin is acutely involved in the estrous phase of FSH release in the rat just as noradrenalin exerts other effects on the hypothalamic control of anterior pituitary gland hormone secretion (Van Loon, 1973; Martin, 1976; Fuxe et a!., 1979). In view of the possibility that the rat brain could play an acute role in the estrous phase of FSH release and in view of some of the differences which appear to exist in the neural control of the estrous phase of FSH release between rats and hamsters, it is important to study further the role of the rat brain in this event. In the present study, we have investigated whether the estrous phase of FSH release in the rat is dependent on the immediate presence of any neural input to the MBH. MATRIALS AND MTHODS Female Sprague-Dawley rats were purchased from Simonsen Laboratories, Inc. (Gilroy, CA), housed in a temperature-controlled (24-26#{176}C) room with the lights on from 0500 h to 1900 h daily, and provided food and water ad libitum. Starting 3 weeks alter the rats were first housed in the vivarium, vaginal smears were prepared daily by saline lavage. Rats which exhibited 2 or more consecutive 4-day estrous cyles were used (body weight range was 204 g to 300 g). A cannula was inserted through the right external jugular vein in all rats as described by Terkel (1972) under brief exposure to ether fumes between 1200 h and 1300 h of proestrus. Six rats were bled (0.8 ml) through the cannula at 1400 h of proestrus and FSH and LH concentrations were measured in the plasma to determine presurge plasma FSH and LH levels at h of proestrus. Additional cannulated rats were untreated or subjected to sham or complete deafferentation of the MBH. These rats were bled (0.8 ml) at 2200 h of proestrus and 0200 h, 0600 h, 1000 h, 1010 h and 1030 h of estrus. Fifty ng of LH releasing hormone (LHRH; Beckman Instruments, Palo Alto, CA; lot no. O114) was injected through the cannula immediately after taking the blood sample at 1000 h of estrus. Blood was collected into heparinized syringes and then placed into heparinized tubes to prevent clotting of the samples. The MBH was surgically isolated from the rest of the brain using ether as an anesthetic between 2000 h and 2130 h of proestrus. The methods employed have been described previously in detail (Blake and Sawyer, 1974). In brief, the knife was lowered at 1.4 mm posterior to bregma to the base of the brain and rotated 90#{176} to the right, the stereotaxic carrier was moved posteriorly 2.0 mm, the knife was rotated 180#{176} to the left, the stereotaxic carrier was moved anteriorly 2.0 mm, and the knife was moved 90#{176} to the right and then removed from the brain. The dimensions of the knife used were 1.8 mm radius and 1.8 mm vertical. Sham cuts were performed by lowering the knife in the midline to the corpus callosum at 1.4 mm posterior to bregma and withdrawing the knife. Rats were killed after the bleeding at 1030 h of estrus. The oviducts were excised and examined under a microscope to determine if the ampullae were swollen and if ova were present in the ampullae. The brain of rats with deafferented hypothalami were carefully removed and stored in 10% buffered formalin. The ventral surfaces of all these brains and frontal sections of some of these brains were carefully examined with a light microscope to determine if: a) the cuts were completely through the ventral surface of the brain; b) the cuts were symmetrical with respect to midline; and c) the anterior border of the cut was immediately posterior to the optic chiasm. Five of 14 rats did not meet these criteria and were eliminated from the study. An additional 2 rats were eliminated from the study since the pituitary glands were nonfunctional as evidenced by the failure of LHRH to elevate the plasma FSH or LH concentrations. Plasma FSH was measured with the materials supplied with the FSH assay kit distributed by NIAMDD by the method of Niswender et al. (1968). Luteinizing hormone was measured as described by Niswender et al. (1968) using NIAMDD-rat LH-RP-1 as a standard. A serum pool was measured in quadruplicate in a single assay for each hormone. The within-assay coefficients of variation were 7.7% and 2.6% for FSH and LH respectively. Statistical analyses of the data were made using one- or two-way analysis of variance (for repeated measures where appropriate). Post-hoc Newman-Keuls tests were subsequently performed and P values <0.05 were considered statistically significant.
3 HYPOTHALAMUS AND STROUS FSH RLAS 401 C) C I Cl) LI. Naive (n=6) #{149}#{149} u Sham Cut (n=8 a--a Complete Cut (n=7) (I) a. 5Ong * LHRH Time of Day FIG. 1. ffects of sham or complete deafferentation of the medial basal hypothalamus between 2000 h and 2130 h of proestrus on mean plasma FSH concentrations from 2200 h of proestrus to 1000 h of estrus in rats bled serially through an atrial cannula. Fifty ng of LHRH was injected through the cannula at 1000 h of estrus. The 2 dash-dot lines designate the range of presurge plasma FSH levels at 1200 h of proestrus in 6 additional rats. Standard errors are not plotted for the middle of the 3 points at each time period to facilitate visualization of the data. RSULTS Mean plasma FSH concentrations at all time periods between 2200 h of proestrus and 1000 h of estrus in all 3 groups of serially bled rats were higher (P<0.O1) than presurge levels of FSH in other rats at 1400 h of proestrus (Fig. 1). In all 3 groups of serially bled rats, plasma FSH concentration rose between 2200 h of proestrus and 0200 h of estrus (P<0.05) and declined between 0200 h and 0600 h of estrus (P<O.05) and between 0600 h and 1000 h of estrus (P<0.01). There were no statistically significant differences in plasma FSH concentrations between any of the 3 groups at any of the time periods. Mean plasma LH concentrations at 2200 h of proestrus in a!! 3 groups of serially bled rats were higher (P<0.01) than presurge levels of LH in other rats at 1400 h of proestrus (Fig. 2). Plasma LII levels then declined to approach or reach presurge LH levels by 0200 h of estrus. There were no statistically significant differences in plasma LH concentrations between any of the 3 groups at any of the time periods. Injection of 50 ng of LHRH at 1000 h of estrus caused the plasma FSH (Fig. 1) and LB (Fig. 2) levels to rise in all 3 groups within 10 mm (P<O.01) and to remain significantly elevated (P<0.05) at 30 mm after injection. There were no statistically significant differences in the plasma FSH or LH responses between any of the groups. All rats ovulated with 9 to 15 ova. There were no differences in the number of ova shed between groups. In the 5 rats eliminated from the study due to incomplete deafferentation of the MBH or the improper placement of cuts, the plasma FSH concentrations from 2200 h of proestrus to 1000 h of estrus were not different (P<0.05) from those of rats with properly placed cuts. In the 2 rats eliminated on the basis of their failure to show an FSH or LH response to LHRH, plasma FSH concentrations were low (<200 ng/ml) from 0200 h to 1000 h of estrus. DISCUSSION The results of this study clearly indicate that the estrous phase of FSH release in the cyclic rat occurs in the absence of acute neural input
4 402 RUSH T AL #{149}-#{149}Naive (n=6) #{149} Sham Cut (n 8) 50n 4 a 0 LHRH #{149}S it 1600 Complete Cut (n=l) 0) C I 1 U, a Time of Day FIG. 2. ffects of sham or complete deafferentation of the medial basal hypothalamus between 2000 h and 2130 h of proestrus on mean plasma LH concentrations from 2200 h of proestrus to 1000 h of estrus in rats bled serially through an atrial cannula. Fifty ng of LHRH was injected through the cannula at 1000 h of estrus. The 2 dash-dot lines designate the range of presurge plasma LH levels at 1400 h of proestrus in 6 additional rats. Note the break on the ordinate scale. The stars at 0600 h and 1000 h of estrus indicate that the mean value for all 3 groups was between 15 and 20 ng/ml. Standard errors at 1000 h of estrus are not plotted to facilitate visualization of the data. to the MBH. Complete surgical disconnection of the neural afferents to the MBH during the evening of proestrus had no effect on the high plasma FSH concentrations during late proestrus and the morning of estrus. The results cannot be readily explained by hypothesizing the diffusion of chemicals or hormones from the severed neurons across the cut to the MBH or by damage to the neurons within the MBH. Under such circumstances, one would expect LHRH to be released. As the plasma LH response to either a pulse injection or constantrate i.v. infusion of LHRH during the late evening of proestrus is as great as it is during the early afternoon of proestrus (Blake, 1974, 1976), one might expect the plasma LH concentrations to be elevated above control values at 2200 h of proestrus and possibly during the morning of estrus. The plasma LH levels were not elevated at these times in the rats with deafferented hypothalami. Also, the results cannot be readily explained by hypothesizing that our surgical procedure interfered with the integrity of the anterior pituitary gland. The plasma LH and FSH responses to LHRH in rats with deafferented hypothalami were not different from those of the controls. Our results are in agreement with studies conducted in hamsters in which complete deafferentation of the MBH during the early evening of proestrus had no effect on the estrous phase of FSH release (Chappel et a!., 1977). Having eliminated the possibility that extrahypotha!amic brain regions play an acute role in causing the estrous phase of FSH release, it remains to be determined whether the MBH plays any acute role in the estrous phase of FSH release in the rat. There is evidence which indicates that LHRH plays no acute role in the estrous phase of FSH release. Administration of anti-lhrh serum from rabbits or from sheep to rats during the evening of proestrus did not affect the estrous phase of FSH release (Hasegawa eta!., 1981; Blake and Ke!ch, 1981). The dosages of antiserum employed should
5 HYPOTHALAMUS AND STROUS FSH RLAS 403 have been sufficient to inactivate any biologically active LHRH during the morning of estrus as administration of the same dosages around noon of proestrus completely blocked the preovulatory plasma LB surge and the proestrous phase of FSH release (Hasegawa et al., 1981; Blake and Kelch, 1981). Also, one need not speculate as to the existence of another hypothalamic hormone which releases FSH preferentially to LII in order to explain the estrous phase of FSH release. The secretion of FSH during estrus is likely due, at least to a substantial extent, to an increase in the basal FSH secretion rate (secretion independent of the immediate presence of any hormones of nonanterior pituitary gland origin). Anterior pituitary glands removed from rats during the late evening of proestrus or the morning of estrus and incubated in culture for 2 h, released substantially more FSH than did anterior pituitary glands removed from rats at other times during the estrous cycle (lias and Blake, 1981). xperiments are currently underway to determine more conclusively whether the MBH plays any acute role in causing the estrous phase of FSH release in the rat. ACKNOWLDGMNTS We thank Drs. Albert F. Parlow, Gordon D. Niswender and Leo Reichert, Jr., as well as the Rat Pituitary Hormone Program of the NIAMDD for their generous gifts of materials used to assay FSH and LH. RFRNCS Ashiru, 0. A. and Blake, C. A. (1978). Restoration of the periovulatory follicle-stimulating hormone surges in sera by luteinizing hormone releasing hormone in phenobarbital-blocked rats. Life Sri. 23 : Blake, C. A. (1974). Differentiation between the critical period, the activation period and the potential activation period for neurohumoral stimulation of LH release in proestrous rats. ndocrinology 95: Blake, C. A. (1976). Simulation of the proestrous luteinizing hormone (LH) surge alter infusion of LH-releasing hormone in phenobarbital-blocked rats. ndocrinology 98: Blake, C. A. and Kelch, R. P. (1981). Administration of anti-lhrh serum to rats: effects on periovulatory secretion of luteinizing hormone and follicle-stimulating hormone. ndocrinology 109: Butcher, R. L., Collins, W.. and Fugo, N. W. (1974). Plasma concentrations of LH, FSH, prolactin, progesterone and estradiol-17p throughout the 4-day estrous cycle of the rat. ndocrinology 94: Chappel, S. C., Norman, R. L. and Spies, H. G. (1977). Regulation of the second (estrous) release of follicle-stimulating hormone in hamsters by the medial basal hypothalamus. ndocrinology 101: Chappel, S. C., Norman, R. L. and Spies, H. G. (1979). vidence for a specific neural event that controls the estrous release of follicle-stimulating hormone in golden hamsters. ndocrinology 104: Daane, T. A. and Parlow, A. F. (1971). Periovulatory patterns of rat serum follicle stimulating hormone and luteinizing hormone during the normal estrous cycle: effects of pentobarbital. ndocrinology 88: lias, K. A. and Blake, C. A. (1981). A detailed in vitro characterization of the basal folliclestimulating hormone and luteinizing hormone secretion rates during the rat 4-day estrous cycle. ndocrinology, 109: Fuxe, K., Andersson, K., Agnati, L F., Ferland, L., Hokfelt, T., neroth, P., Gustaffson, J.-A. and Skett, P. (1979). Central catecholamine systems and neuroendocrine regulation. Controllers of anterior pituitary secretion. In: Catecholamines: Basic and Clinical Frontiers, Vol. 2 (. Usdin, I. J. Kopin and J. Barchas, eds.). Pergamon Press, Oxford, pp Hasegawa, V., Miyamoto, K., Vazaki, C. and lgarashi, M. (1981). Regulation of the second surge of follicle-stimulating hormone; effects of antiluteinizing hormone-releasing hormone serum and pentobarbital. ndocrinology 109: Martin, J. B. (1976). Brain regulation of growth hormone secretion. In: Frontiers in Neuroendocrinology, Vol. 4 (L. Martini and W. F. Ganong, eds.). Raven Press, New York. pp Niswender, G. D., Midgley, A. R. Jr., Monroe, S.. and Reichert, L.. Jr., (1968). Radioimmunoassay of rat luteinizing hormone with anti-ovine LH serum and ovine LH- 3 I. Proc. Soc. xt. Biol. Med. 128: Rush, M.., Ashiru, 0. A. and Blake, C. A. (1980). Hypothalamic-pituitary interactions during the periovulatory secretion of follicle-stimulating hormone in the rat. ndocrinology 107: Siegel, H. I., Bast, J. D. and Greenwald, G. 5. (1976). The effects of phenobarbital and gonadal steroids on periovulatory serum levels of luteinizing hormone and follicle stimulating hormone in the hamster. ndocrinology 98: Smith, M. S., Freeman, M.. and Neill, J. D. (1975). The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the rat: prolactin, gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy. ndocrinology 96: Terkel, J. (1972). A chronic cross-transfusion technique in freely-behaving rats using a single heart catheter. J. AppI. Physiol. 3 3: Van Loon, G. R. (1973). Brain catecholainines and ACTH secretion. In: Frontiers in Neuroendocrinology, Vol. 3 (W. F. Ganong and L. Martini, edsj. Oxford University Press, New York, pp Weiner, R. I., Shryne, J.., Gorski. R. A. and Sawyer, C. H. (1972). Changes in the catecholamine content of the rat hypothalamus following deafferentation. ndocrinolojy 90:
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