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1 Center for Neuroendocrine Studies, Neuroscience and Behavior Program, and Department of Psychology, University of Massachusetts, Amherst, Massachusetts 01003-7720; and 2 Department of Biological Sciences, Lehigh University, Bethlehem, Pennsylvania 18015
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ABSTRACT |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Food deprivation inhibits ovulatory cycles and estrous behavior in Syrian hamsters. Lesions of the area postrema (AP) prevented the suppression of estrous behavior in food-deprived hamsters, but they did not prevent the suppression of estrous cyclicity or the increase in running-wheel activity caused by food deprivation. Food deprivation or treatment with pharmacological inhibitors of glycolysis and fatty acid oxidation decreased estrogen-receptor immunoreactivity (ERIR) in the ventromedial hypothalamus (VMH), increased ERIR in the arcuate nucleus (Arc) and the posterior parvicellular paraventricular nucleus (PaPo), but had no effect on ERIR in the posterodorsal medial amygdala or the anterior parvicellular paraventricular nucleus. Lesions of the AP prevented the food deprivation-induced decrease in VMH ERIR and the increase in Arc ERIR, but they did not prevent the increase in ERIR in the PaPo. Thus, whatever physiological cues are produced by food deprivation, an intact AP is required for their transmission to the neural circuits controlling estrous behavior, VMH ERIR, and Arc ERIR. The AP is not essential for transmission of this information to the neural circuits controlling estrous cyclicity, running-wheel activity, or PaPo ERIR.
ventromedial hypothalamus; arcuate nucleus; paraventricular nucleus; amygdala; estrogen receptor
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INTRODUCTION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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THE AVAILABILITY OF AN ample supply of oxidizable metabolic fuels is a requirement for successful mammalian reproduction (3). In female mammals of all species studied to date, including human beings, reproduction is particularly sensitive to the availability of metabolic fuels. When food availability is restricted or there is an increase in fuel demand that is unaccompanied by a compensatory increase in caloric intake, nutritional infertility ensues. This can manifest itself in a number of ways, including a delay in the onset of puberty, suppression of ovulatory cycles and estrous behavior in adult animals, a reduction in lactational performance, and an inhibition of maternal behavior (for review see Refs. 3, 31).
In Syrian hamsters, 48 h of food deprivation starting just after estrus (on days 1 and 2 of the estrous cycle) prevents the occurrence of the next expected estrus, but deprivation on any other 2 days of the cycle is ineffective (16). Decreased availability of metabolic fuels for 48 h, caused either by food deprivation or by treatment with metabolic inhibitors such as 2-deoxy-D-glucose (2-DG) and methyl palmoxirate (MP), which cause glucoprivation and lipoprivation, respectively, suppresses steroid-induced estrous behavior in ovariectomized hamsters (4). The effects of metabolic fuel availability on estrous cycles seem to be separate and independent from those on estrous behavior. Indeed, hamster estrous cycles can be inhibited by glucoprivation alone, whereas suppression of estrous behavior requires a combination of both glucoprivation and lipoprivation (4, 23).
The search for neural pathways by which peripheral metabolic status is conveyed to the forebrain circuits controlling reproduction has been guided by research on the neural circuitry that regulates eating behavior in rats (20). This work shows that the area postrema (AP), the nucleus of the solitary tract (NTS), and the vagus nerves play a significant role in transmitting metabolic information to the forebrain (20). With regard to reproduction, AP lesions block metabolic inhibitor-induced suppression of estrous behavior, as well as the associated decrease in estrogen-receptor immunoreactivity (ERIR) in the ventromedial hypothalamus (VMH). On the other hand, subdiaphragmatic vagotomy abolishes the effects of metabolic inhibitors on ERIR in the medial preoptic area (mPOA) without affecting either lordosis or VMH ERIR (14). These data suggest that estrogen-binding cells in the VMH, critical for induction of lordosis in hamsters, receive information about metabolic fuel availability via the AP, but not the vagus nerves. Similarly, AP lesions, but not vagotomy, block 2-DG-induced inhibition of estrous cycles in Syrian hamsters (24-26). Thus the AP seems to play an essential role in glucoprivic and lipoprivic effects on estrous behavior and in glucoprivic suppression of estrous cycles in Syrian hamsters.
A significant issue not addressed in previous experiments is the role of the AP in mediating the effects of food deprivation, as opposed to those of pharmacological agents such as 2-DG and MP. This is important, because in addition to glucoprivation and lipoprivation, food deprivation causes additional physiological changes such as stomach distension and changes in circulating levels of metabolic hormones that could provide information to the neural circuits controlling reproduction. These cues could act via pathways that do not include the AP. Supporting this possibility are data showing that ablation of the AP/NTS does not prevent the effects of food deprivation on food intake in rats (5) even though it does block metabolic inhibitor-induced food intake (20). This could mean that of the multiple cues produced by food deprivation that stimulate food intake, only some act via the AP/NTS in rats. In the following experiments we determined whether an intact AP is required to convey the inhibitory effects of 48 h of food deprivation on estrous behavior, neural ERIR, and estrous cycles in Syrian hamsters.
Changes in neural estrogen receptors may play a role in the effects of metabolic fuel restriction on reproduction. In ovariectomized hamsters, 48 h of food deprivation, treatment with 2-DG + MP, or acute withdrawal of insulin all cause a significant decrease in the number of detectable ERIR cells in the VMH, an increase in detectable ERIR cells in the mPOA, and no change in the NTS (14). Mapping of additional neural sites where ERIR cells are influenced by restriction of metabolic fuels and determining the direction of the response are essential to discerning a relation between specific neural sites and changes in estrogen-dependent behavioral and neuroendocrine events leading to nutritional infertility. In the following experiments, we examine the effects of 48 h of food deprivation or treatment with metabolic inhibitors on ERIR in several other neural regions that have been implicated in the control of reproductive function, energy balance, or both, including the posterior parvicellular paraventricular nucleus (PaPo), the anterior parvicellular paraventricular nucleus (PaMP), the posterodorsal medial amygdala (MePD), and the arcuate nucleus (Arc) (Fig. 1).
Food deprivation affects numerous nonreproductive behaviors, including locomotor activity, which increases during food deprivation in hamsters and other species (2). We also determined whether the AP is essential for the increase in locomotor activity in food-deprived hamsters.
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METHODS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Animals and Housing
Female Lak:LVG Syrian hamsters weighing 70-80 g were purchased from Charles River Breeding Laboratories (Wilmington, MA) and housed in stainless steel, wire-bottom cages. The animals were housed in a 14:10-h light-dark cycle (lights on at 0600 h) at an ambient temperature of 22 ± 2°C. Purina laboratory rodent chow (no. 5001; Ralston-Purina, St. Louis, MO) was given ad libitum unless otherwise indicated. Water was available at all times. Animals were given 1 wk to acclimate to the laboratory, and then they were bilaterally ovariectomized (except for expt 3) under pentobarbital sodium anesthesia (80 mg/kg ip). Two weeks of recovery were allowed before the start of each experiment. All procedures were conducted in accordance with the National Institutes of Health (NIH) Guide for the Care and Use of Laboratory Animals and were approved by the University of Massachusetts Institutional Animal Care and Use Committee.AP Lesions
AP lesions were performed as described previously (14). Hamsters were anesthetized with pentobarbital sodium (80 mg/kg ip) and positioned in a stereotaxic instrument. An incision was made in the dorsal neck region to expose the muscles underneath. Using blunt dissection, the skull was exposed, and the occipito-atlantal ligament, the dura mater, and the arachnoid membranes were incised to reveal the occipital foramen magnum. The overlying meninges were removed to expose the fourth ventricle, and the AP was aspirated using a 5-µl Wiretrol (Drummond Scientific, Broomall, PA). Surgical wounds were closed with silk. Sham lesions were performed by exposing the dorsal hindbrain.Histology
AP-lesioned animals were given a lethal dose of pentobarbital sodium (120 mg/kg ip) and perfused with saline for 30 s followed by 2% acrolein for 10 min at a pressure of 100 mmHg and a flow rate of 25 ml/min. The medulla was removed and stored overnight in 0.1 M sodium phosphate buffer containing 20% sucrose. Forty-micrometer coronal sections were cut and stained with thionine. Sections were examined to confirm the presence of the lesion. Animals with incomplete lesions of the AP were omitted from the data analyses, as were animals with significant damage to adjacent neural structures. All the animals included in the study had either no or minimal damage to the underlying NTS.Behavior Testing
Two weeks after AP lesions or sham operations, hamsters were injected subcutaneously with 2.5 µg of estradiol benzoate (EB) followed 44 h later with 500 µg of progesterone (P). They were tested for lordosis 4 h after the injection of P in the presence of an experienced male hamster in a Plexiglas arena. Lordosis was quantified by recording the number of seconds spent by the female in the lordosis posture during a 3-min test. To provide a consistent level of flank stimulation to elicit lordosis, a soft 1-cm artist's paint brush was used to stroke the female's flank region during the test period (30).Immunocytochemistry
Hamsters used for ERIR mapping were killed with an overdose of pentobarbital sodium and perfused with 2% paraformaldehyde and 0.4% glutaraldehyde. Brains were then processed for estrogen-receptor immunocytochemistry as described previously (13). In each experiment, all sections from all animals were processed simultaneously. In brief, 40-µm coronal brain sections were incubated with the H-222 monoclonal primary antibody (Abbott Laboratories, North Chicago, IL) at a concentration of 1 µg/ml for 72 h. They were then incubated with the secondary antiserum, biotinylated rabbit anti-rat immunoglobulin, at a concentration of 6 µg/ml for 90 min. The sections were then incubated for another 90 min in avidin-DH-biotinylated horseradish peroxidase-H complex and reacted with diaminobenzidine in the presence of hydrogen peroxide to give a dark brown-colored end product indicating the presence of estrogen receptors.Two sections, separated by 120 µm, from each brain area (Fig. 1) were chosen from each animal after careful matching of their landmarks under dark-field illumination. The only exception was in the Arc in expt 2, where only one closely matched section per animal was available. The experimenter was always blind to the treatment groups of the sections being analyzed. ERIR cells were counted with a computer-aided image analysis system using the public-domain NIH Image program (developed at the NIH and available on the Internet at http://rsb.info.nih.gov/nih-image/). At the beginning of the analysis of the first sample, the camera gain and black levels were adjusted to give a normal distribution of gray levels ranging from 0 to 255, falling within the parameters of the imaging system. This light level was maintained throughout the analysis to obtain consistent measurements. The mean pixel density and standard deviation for each section was determined, and the criterion for a labeled cell nucleus to be counted was set at two standard deviations above the mean pixel density of the region to be analyzed.
Immunostaining depends on the antibody-receptor interactions in the cell, and the intensity of immunostaining is believed to be proportional to the concentration of receptors. Previous studies have shown that increased optical density can be used as an index for increased antigen concentrations (1). In brain regions where we did not find differences in the total count of ERIR cells between treatments, they were further analyzed for differences in the staining intensity. This was calculated from each cell's darkest pixel. Cells were categorized into two groups with maximum pixel densities (i.e., optical densities) of >90 and >200.
Analyses of Data
Differences in the total number of detectable ERIR cells and maximum pixel densities within specific brain sites from each treatment group were analyzed by t-tests or one- or two-way analyses of variance. Estrous behavior scores were analyzed by two-way analyses of variance. Significant treatment group effects were further analyzed by Newman-Keuls post hoc tests. Estrous cyclicity data were analyzed by Fisher's exact probability test. All tests were based on two-tailed tests of significance, and results were considered significant if P < 0.05.Procedures
Experiment 1. The first experiment determined the effect of metabolic fuel restriction, either by food deprivation or by treatment with inhibitors of glycolysis (2-DG) and fatty acid oxidation (MP), on ERIR in four neural sites not examined previously: PaPo, PaMP, MePD, and Arc (Fig. 1). Ovariectomized hamsters were divided into three groups: 1) food deprived for 48 h (n = 5), 2) fed ad libitum and given a combination of 2-DG [750 mg/kg (1 ml/kg) ip] and MP [25 mg/kg (10 ml/kg) by gavage] every 6 h for 48 h (n = 5), and 3) fed ad libitum and treated with the respective vehicles (0.9% saline for 2-DG and 0.5% methyl cellulose for MP) (n = 5). They were then perfused and prepared for estrogen-receptor immunocytochemistry as described above. The immunostaining in PaPo was lighter compared with other brain regions both in the control and treatment groups. To obtain a better contrast, a filter (Wratten filter no. 44) was used on all sections for analyzing PaPo ERIR (32).
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Experiment 2. The second experiment evaluated the effect of AP lesions on ERIR in the VMH, Arc, and PaPo of food-deprived animals. Ovariectomized hamsters were given aspiration lesions of the AP (n = 20) or were sham operated (n = 10). Two weeks later, half of the animals in each group were either fed ad libitum or food deprived for 48 h and then perfused for estrogen-receptor immunocytochemistry.
Experiment 3. The third experiment examined the effect of AP lesions on suppression of steroid-induced lordosis in food-deprived animals. Two weeks after ovariectomy, animals were given aspiration lesions of the AP (n = 35) or were sham operated (n = 15). Two weeks later, all animals were tested for estrous behavior as described above. Half of the animals in each group were food deprived during the 48 h between EB injection and behavioral testing; the other half were fed ad libitum.
Two weeks later, the same animals were used to examine the effect of AP lesions on deprivation-induced increases in locomotor activity. Running wheels (16.5 cm diameter) were attached to the stainless-steel tops of conventional rodent polycarbonate cages and connected to a microcomputer. Four large boxes, each accommodating up to eight individual activity cages, were equipped with fluorescent lights. Total revolutions in successive 5-min time bins were stored continuously and later downloaded for determination of 24-h activity totals (10). AP-lesioned or sham-lesioned animals were adapted to running wheels for 7 days. Then all food was removed for the next 3 days. Activity of the two treatment groups before and during the food deprivation period was recorded.
Experiment 4. The fourth experiment analyzed the effect of AP lesions on suppression of estrous cyclicity in food-deprived animals. Estrous cycles of gonadally intact hamsters were monitored for characteristic postovulatory vaginal discharge (18) for 2 wk. Those animals with irregular estrous cycle were omitted from the study. Regularly cycling animals were given aspiration lesions of the AP (n = 11) or were sham lesioned (n = 9). Monitoring of estrous cycles resumed until all the animals showed two consecutive cycles. All animals were then subjected to 48 h of food deprivation (estrous cycle days 1 and 2). Animals were examined daily until they showed the postovulatory vaginal discharge. Monitoring was continued until all the animals showed two consecutive estrous cycles or 15 days had elapsed since the last vaginal discharge.
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RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Experiment 1: ERIR in Fed, Food-Deprived, and 2-DG + MP-Treated Hamsters
Food deprivation or 2-DG + MP treatment caused similar changes in neural ERIR within each brain area examined. The number of detectable ERIR cells in the PaPo increased significantly following food deprivation or treatment with 2-DG + MP compared with ad libitum-fed control animals (Fig. 2). In contrast to the PaPo, ERIR in the PaMP and MePD did not respond to decreases in fuel availability either in the number of detectable ERIR cells (Fig. 2) or in the intensity of estrogen receptor immunostaining. In the Arc, there was no change in the total number of detectable ERIR cells, but there was a significant increase in the number of darkly stained cells in both the food-deprived and 2-DG + MP-treated animals (Fig. 3).
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Experiment 2: Effect of AP Lesions on Neural ERIR in Food-Deprived Hamsters
Twelve of twenty animals sustained complete destruction of the AP. The final group sizes were sham lesioned, fed, n = 5; AP lesioned, fed, n = 6; sham lesioned, deprived, n = 5; and AP lesioned, deprived, n = 6. In sham-lesioned animals, 48 h of food deprivation resulted in a significant decrease in ERIR in the VMH and a significant increase in ERIR in the Arc and in the PaPo (Fig. 4). AP lesions abolished the effects of food deprivation on VMH and Arc ERIR but did not prevent the effect of deprivation on PaPo ERIR (Fig. 4).
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Experiment 3: Estrous Behavior and Running Wheel Activity in AP-Lesioned, Food-Deprived Hamsters
Twenty-seven of thirty-five animals sustained complete destruction of the AP. The final group sizes were sham-lesioned, fed, n = 8; sham-lesioned, deprived, n = 10; AP-lesioned, fed, n = 14; and AP-lesioned, deprived, n = 13. Neurologically intact animals showed the expected suppression of estrous behavior following food deprivation, but AP lesions blocked the inhibitory effect of food deprivation on lordosis duration (Fig. 4).Baseline running wheel activity of both sham-lesioned and AP-lesioned groups was similar. AP lesions did not have any effect on the increase in locomotor activity induced by food deprivation. Food deprivation significantly increased the running wheel activity of all the animals at all the time points, regardless of whether or not they had AP lesions (Fig. 5).
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Experiment 4: Estrous Cyclicity in AP-Lesioned, Food-Deprived Hamsters
Eight of eleven animals sustained complete destruction of the AP. The final group sizes were sham-lesioned, n = 9; AP-lesioned, n = 8. Each animal served as its own control before it was food deprived. All the animals, both sham-lesioned and AP-lesioned, showed normal 4-day estrous cycles before they were food deprived. Hence, it was clear that surgery did not adversely affect estrous cyclicity. AP lesions did not block the inhibitory effect of food deprivation on estrous cyclicity (Fig. 6).
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Lesions of the AP abolish the effects of inhibitors of glucose and fatty acid oxidation (2-DG + MP) on estrous behavior and VMH ERIR in hamsters (14). However, the presence or absence of food generates a wide variety of potential signals to the brain other than glucose and fatty acid oxidation. These other potential cues include oral stimulation, gut fill, rate of gastric emptying, release of hormones such as cholecystokinin and insulin, the release of digestive enzymes and cofactors, and changes in the plasma profiles of amino acids and other metabolites. Thus it is conceivable that AP lesions could prevent the effects of 2-DG + MP on lordosis and VMH ERIR, but not of food deprivation with its wider range of physiological signals. Indeed, with the eating behavior in rats, a disparity in response is seen with 2-DG + MP treatment versus food deprivation (5, 20). However, our findings clearly show that lesions of the AP prevent the effects of 48 h of food deprivation on sexual receptivity and ERIR in the VMH and in the Arc. Therefore, if there are physiological cues in addition to glucoprivation and lipoprivation that affect sexual receptivity and VMH or Arc ERIR during food deprivation, they too require an intact AP to have their effects.
It is unlikely that these effects of the AP lesions are due to a functional vagotomy as a consequence of inadvertent damage to the NTS. AP lesions prevented the effects of food deprivation even in the animals with no NTS damage. In addition, total subdiaphragmatic vagotomy does not prevent the effects of 2-DG + MP treatment on sexual receptivity or VMH ERIR (14).
AP lesions did not prevent several other responses to food deprivation, including the suppression of estrous cyclicity, increased PaPo ERIR, and increased running wheel activity. AP lesions completely abolish 2-DG-induced suppression of estrous cyclicity (26), in contrast to the present data. Thus additional cues that result from food deprivation seem to reach forebrain circuits controlling estrous cyclicity via pathways that do not include the AP. Vagotomy does not block 2-DG- or MP-induced suppression of cyclicity in hamsters (24, 25), but it is conceivable that some of the other food deprivation-induced cues could reach the forebrain via vagal afferents. It is likely that the metabolic fuel information is transmitted via the vagus nerves to PaPo ERIR neurons (6), as is the case with mPOA (14). The effect of vagotomy on the food deprivation-induced increase in running wheel activity remains to be determined.
Food deprivation caused changes in the number of detectable ERIR cells within the different hypothalamic nuclei examined. The changes are site specific, because 48 h of food deprivation decreased the number of detectable ERIR cells in the VMH, increased the number of detectable ERIR cells or the intensity of immunostaining in the PaPo and Arc, and had no effect in the MePD or PaMP. These food deprivation-induced changes were mimicked by the pharmacological inhibition of glucose and fatty acid oxidation by 2-DG + MP treatment. These findings complement previous work showing that food deprivation or treatment with 2-DG + MP decreases the number of detectable ERIR cells in the VMH, increases them in the mPOA, and has no effect in the NTS (14).
Food deprivation affects neural estrogen receptors in species other than hamsters. Underfeeding for 48 h results in a decrease in the ERIR in the VMH, mPOA, and Arc in prepubertal female mice (21). In female rats, 48 h of food deprivation results in an increase in ERIR in the paraventricular nucleus (PVN) and A2 region of the NTS (7). These findings indicate that nutritional status can influence neural ERIR in a number of species, both in adults and in prepubertal animals, consistent with a significant role for estrogen receptors in mediating the effects of fuel restriction on fertility.
By virtue of its connections, the PVN has the potential to influence both neuroendocrine and autonomic mechanisms (15). It is conceivable that changes in estrogen receptors in the PVN may mediate some of the effects of nutritional challenges on reproduction. Indeed, some data suggest that estrogen feedback at the PVN is essential to reduce luteinizing hormone (LH) pulsatility during fasting in rats (17). It is interesting to note that the ERIR in two regions of the parvicellular subdivision of the PVN responded differently to metabolic fuel restriction. Retrograde tracing in rats illustrates that the primary projections of labeled cells in the subnuclei of the parvicellular PVN corresponding to where we counted the estrogen receptors in hamsters are different. For example, labeled cells in the lateral parvicellular part, which corresponds to the PaPo, project primarily to the dorsal medulla and spinal cord, and the medial parvicellular cells, which correspond to the PaMP, project mainly to the median eminence (28). It is plausible that estrogen-binding neurons in these two regions of the parvicellular subdivision of the PVN participate in separate effects of fuel restriction.
The medial nucleus of the amygdala has been implicated in the control of estrous behavior (19). It has afferent and efferent connections with various regions specifically involved in reproduction in hamsters (11). The posterodorsal part of this nucleus (MePD) contains a large number of ERIR cells in rats (27) and hamsters (13), and mating behavior induces selective expression of Fos protein in MePD in female rats (29). In addition, MePD has been implicated as a temporal lobe site involved in the regulation of food intake and body weight (12). However, ERIR cells in MePD appear to have minimal participation in fasting-induced infertility.
Although food deprivation did not alter the number of detectable ERIR cells in the Arc, it did increase the intensity of immunostaining, consistent with an increase in estrogen receptor content. The Arc is a site where estradiol exerts negative feedback effect on LH secretion, and it contains cell bodies containing neuropeptides such as neuropeptide Y, galanin, and opioids, which are colocalized with estrogen receptors in rats (8, 9, 22). Further studies are needed to determine whether metabolic fuel deprivation selectively affects ERIR in any particular type of neuropeptide-producing cells in the Arc of hamsters.
In summary, AP lesions abolished the inhibitory effect of food deprivation on estrous behavior and VMH ERIR, clearly showing that AP mediates the effect of food deprivation on these measures. Other effects of food deprivation, including suppression of estrous cyclicity, increased ERIR in the PaPo, and increased running-wheel activity, were not influenced by AP lesions, suggesting that these responses are mediated through alternate pathways. In addition, food deprivation caused increases in ERIR in PaPo and Arc, but the MePD and PaMP were unaffected.
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ACKNOWLEDGEMENTS |
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We thank Robin Lempicki and Jay Alexander for expert technical assistance, Eric Corp for comments on the manuscript, and Abbott Laboratories for providing the H-222 antibody.
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FOOTNOTES |
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This work was supported by Research Grants NS-10873, MH-01096, DK-53402, and HD-30372 and Senior Scientist Award MH-00321 from the National Institutes of Health and Research Grant IBN9723938 from the National Science Foundation.
Address for reprint requests: G. N. Wade, Dept. of Psychology, Univ. of Massachusetts, Amherst, MA 01003-7710.
Received 31 October 1997; accepted in final form 24 March 1998.
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Discussion
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