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Lordosis behavior in male rats after lesions in different regions of the corticomedial amygdaloid nucleus
HORMONES
AND
BEHAVIOR
23, 448-455 (1989)
Lordosis Behavior in Male Rats after Lesions in Different Regions of the Corticomedial Amygdaloid Nucleus D. CHATEAU ANDCL. Institute
of Histology, Faculty of Medicine, and URA 99 CNRS, Strasbourg,
ARON University Louis Pasteur, 67000, France
The aim of the experiment was to study the effects of stereotaxic lesions of the anterior and the posterior regions of the corticomedial amygdaloid nucleus (CMN) on the display of lordosis behavior by the male rat. Animals were orchidectomized as adults and given estradiol benzoate and progesterone (P) sequentially. Sexual behavior testing was performed by 9 2 1 hr after P injection. Lesions placed into the posterior region of the CMN significantly decreased the proportion of animals showing lordosis behavior as compared to sham-operated and control animals. By contrast lesions in the anterior region of the CMN did not cause any changes in the proportion of animals displaying lordosis but markedly increased the lordosis quotient (LQ) of responding animals. The CMN was then concluded to exert a dual control in the display of lordosis behavior in the male rat with a posterior region regulating the willingness of animals to display lordosis behavior and rostra1 region subserving inhibitory mechanisms related to the sexual performance (LQ values). Q 1989 Academic press. IJK.
Previous experiments in our laboratory (Schaeffer and Aron, 1981; Chabli, Schaeffer, Samama, and Aron, 1985; Schaeffer, Roos, and Aron, 1986b) showed that heterotypic sexual behavior, which is characterized by lordosis responses to male mounts, could be induced in rats orchidectomized as adults and primed with ovarian hormones. Recently Schaeffer er al. (1986) reported that the expression of lordosis behavior in the male rat is regulated in part by the repressive action of the accessory olfactory bulbs (AOB) and Chateau and Aron (1988) showed that the corticomedial amygdaloid nucleus (CMN) exerts in the male rat a facilitatory role in the control of this behavior. This led to the assumption that in the male rat inhibitory mechanisms originating in the AOB were involved in the control of heterotypic behavior by the CMN. It is well known (Winans ans Scalia, 1970; Scalia and Winans, 197.5) that the CMN receives afferent fibers from both the AOB and the main olfactory bulbs (MOB). The former projects to the posteromedial region of the CMN and the latter to the anterolateral region. In the present study, the respective roles played by the anterior and 448 0018-506X/89 $1.50 Copyright All rights
0 1989 by Academic Press, Inc. of reproduction in any form reserved
AMYGDALA
AND
LORDOSIS
IN MALE
RATS
449
the posterior regions of the CMN in the control of heterotypic sexual behavior of the male rat have been investigated. METHODS Animals
Young unexperienced adult male Wistar rats (220-280 g) bred in our colony were used. They were kept under controlled conditions of lighting (lights on 0200-1600 hr) and maintained at a room temperature of 2224°C. They had free access to a commercial laboratory food and tap water. At 3 months of age the animals were orchidectomized (ORCH) under ether anesthesia and then allowed a week postoperative recovery period. Procedure First experiment. The purpose of the first experiment was to examine the effects of lesions of the posterior region of the CMN on the display of lordosis behavior by the male rat. Following orchidectomy bilateral stereotaxic lesions encompassing the traditionally called medial and cortical amygdaloid nuclei were placed into the posterior region of the CMN (Fig. 1B) by passing a cathodic current of 2 mA for 30 set through an epoxylite-coated stainless-steel electrode (diameter 0.25 mm) insulated except for the cut end. Coordinates were AP 4.8; V 1.8; L 3.8 according to Albe-Fessard, Stutinsky, and Libouban (1966). In a group of shamlesioned animals the electrodes were lowered into the brain to a level immediately above the CMN without passing any current. Unoperated animals served as controls. One to 2 weeks after lesioning all the animals received 25 pg estradiol benzoate (EB) in 0.5 ml olive oil subcutaneously (SC) at 1600 hr. They were given 150 pg progesterone (P) 2 days later at 0800 hr and lordosis behavior was tested on the same day between 1600 and 1800 hr. Second experiment. The second experiment was designed to study the effects of lesions of the rostra1 part of the medial and cortical amygdaloid nuclei with limited extension to the basomedial amygdaloid nucleus (Fig. 1A) on the expression of lordosis behavior by the male rat. A week after orchidectomy stereotaxic lesions (2 mA; 30 set) were made using the following coordinates: AP 6.2; V 1.8; L 3.7 (Albe-Fessard et al., 1966). Sham-lesioned animals served as controls. The schedule of sexual behavior testing was the same as in the preceding group. When the experiments were completed, the animals were killed, the brains were fixed in formalin, and the location and extent of the lesions were determined by microscopic examination of frozen unstained serial sections.
450
CHATEAU
AND ARON
FIG. 1. Reconstruction of representative lesions of the anterior part (A) and of the posterior part (B) of the corticomedial amygdaloid nucleus. a, nuclei amygdalae; abl, n. basalis, pars lateralis; abm, n. basalis, pars medialis; ac, n. centralis: ace, n. corticalis; al, n. lateralis; am, n. medialis. The surface of the lesions (striped area) at the plane of maximum size, as seen in unstained serial sections, was drawn on modified stereotaxic plates of Konig and Klippel’s atlas (1963).
Sexual Behavioral
Testing
The lordosis behavior in ORCH rats was tested for 10 min under a dim light in a round 66-cm-diameter mating arena with plastic walls and floor covered with shavings. The ORCH rats were presented to two intact adult sexually vigorous stimulus males (250-350 g) between 1600 and 1800 hr. We selected males that were shown to be fully active when tested at the end of the light period with highly receptive ovariectomized estrogen-progesterone-primed females. They were allowed a 5-min adaptative period in the mating arena prior to the introduction of the ORCH rat. In accordance with previous studies in males primed with ovarian hormones (Schaeffer and Aron, 1981, 1982) we used the following paradigms to evaluate feminine behavior in ORCH rats; (1) the proportion of animals in a given group displaying at least one lordosis response to male mounts; (2) the lordosis quotient (LQ) as computed in each responding animal by dividing the number of lordosis by the number of
AMYGDALA
AND LORDOSIS IN MALE RATS
451
mounts and multiplying by 100. The mean LQ was calculated for each group of responding animals and served as measurement of the mating performance. STATISTICS
The x2 test was used to compare the proportion of ORCH rats displaying lordosis behavior in the different groups of animals. One-way analysis of variance was used for comparing the LQ values (after angular transformation) and the number of mounts by the stimulus males. RESULTS
Effects of Posterior CMN Lesions The results presented in Table 1 show that posterior CMN lesions markedly reduced the proportion of ORCH animals displaying lordosis responses to male mounts with respect to sham-lesioned and intact control animals (x2 = 10.3; P < 0.01; 2 d!. The mean LQ of responding animals did not statistically differ in lesioned, sham-lesioned, and intact control animals (F(2, 22) = 1.89). Neither did the mean number of mounts displayed by the stimulus males differ in these three groups of animals (F(2, 81) = 0.04). Effects of Anterior CMN Lesions As shown in Table 1 rostra1 CMN lesions did not induce any changes in the proportion of animals displaying lordosis responses to male mounts as compared to sham-operated animals (44.1 and 40.5%, respectively; NS). By contrast LQ values of responding animals appeared higher in lesioned (77.5 2 2.6) than in sham-operated animals (48.0 ? 5.7) (F( 1, 30) = 13.41; P < 0.001). The lesioned animals were mounted more frequently by the stimulus males (9.6 t 0.9) than their sham-operated counterparts (7.5 * 0.5) (F(1, 74) = 4.5; P < 0.05). DISCUSSION
Very recently extended lesions of the CMN were shown (Chateau and Aron, 1988) to completely suppress lordosis behavior in ORCH rats primed with gonadal hormones. This led to the assumption that the CMN was absolutely necessary for the male rat to display lordosis behavior. The present study further implicates the posterior region of the CMN in the control of lordosis behavior by the amygdala in the male rat. We observed that lesions located in the posterior region of the medial and cortical amygdaloid nuclei severely impaired the display of lordosis behavior in ORCH rats given 25 pugEB and 150 ,ug P sequentially. The AOB directly projects fibers to the posterior region of the medial and cortical amygdaloid nuclei (Scalia and Winans, 1975; De Olmos,
2sY** 5.7
77.5 + 48.0 f
15/34 I7/42
(44.1%) (40.5%)
31.0 _t 10.5 48.8 k 5.4 40.1 k 4.0
3/32*” ( 9.3%) IO/24 (41.7%) 12/28 (42.8%)
Mean lordosis quotient t SEM in rats displaying at least one lordosis
” All animals received 25 pg EB (SC)at 1600 hr and 150 pg P [SC) 40 hr later. A Testing with two stimulus maIes by 1 to 2 weeks after lesioning and 9 2 I hr after P injection. * P < 0.05 vs sham. ** P c; 0.01 vs sham and controls. *** P < O.OOLvs sham.
_ll----l__.~~~ Experiment I Posterior CMN Iesians Sham lesions Intact controls Experiment z Anterior CMN lesions Sham lesions
Treatment“
Proportion of ORCH rats displaying lordosis ’
9.6 k 0.9* 7.5 i 0.5
9.6 2 0.8 9.9 Ifr 0.9 Y.7 5 0.7
Mean number of mounts -C SEM displayed by the stimulus malt
TABLE I Effects of Lesions of the Anterior and Posterior Regions of’ the Corticomedial Amygdaloid Nucleus (CMN) on Lordosis Behavior in Orchidectomized (ORCH) Rats Primed with Estradiol Benzoatc (EB) and Progesterone (P)
% 2
z
5 2 s
AMYGDALA
AND
LORDOSIS
IN MALE
RATS
453
Alheid, and Beltramino, 1985) which itself projects fibers to the VMN via the stria terminalis (MacLean, 1985). Recently the ABO has been shown to be involved in the mechanisms governing lordosis behavior in the male rat. Schaeffer et al. (1986b) reported that this olfactory structure exerts an inhibitory influence on the display of lordosis behavior in estrogen-progesterone-treated ORCH rats. Additionally, Chateau, Chabli, and Aron (1987) showed that the VMN represents in the male as in the female (for review, see Pfaff and Schwartz-Giblin, 1988) the target for the activation of lordosis behavior by gonadal hormones. All these findings support the view that the facilitatory control exerted by the VMN on lordosis behavior in the male rat is strictly dependent on the CMN which itself is subjected to the inhibitory control of the AOB. However an important question was whether the rostra1 part of the CMN which receives projections from the main olfactory bulb (De Olmos et al., 1985; MacLean, 1985; Switzer, De Olmos, and Heimer, 1985) might be involved in the control of lordosis behavior in the male rat. The present results provided a clear answer to this question. Although the proportion of animals displaying lordosis behavior was not affected by lesions placed in the rostra1 part of the medial and cortical nuclei, LQ values were markedly enhanced in the animals which showed lordosis responses to male mounts. Indeed animals sustaining lesion of the anterior CMN were mounted more frequently than controls. However, we do not believe that this increased mounting contributed the lesions animals’ increased LQ scores. Previous findings in our laboratory (Chabli et al., 1985; Schaeffer, Chabli, and Aron, 1986a) are consistent with this view. Schaeffer, Al Satli, Kelche, and Aron (1982) observed in ORCH rats primed with gonadal hormones a rise in LQ values following anterior olfactory bulb removal disconnecting bulb remnants from nasal passages, thus suggesting that the sexual performance (LQ values) was regulated by the main olfactory system. Therefore it is tempting to suppose that the rostra1 region of the medial and cortical nuclei constitutes the target for the main olfactory system which conveys olfactory cues to the CMN of the amygdala. The CMN then may be considered as a heterogenous nervous structure exerting a dual control on the display of lordosis behavior in the male rat, with a rostra1 region subserving inhibitory mechanisms related to satiety and a posterior region regulating the willingness of animals to display lordosis behavior. It is worth mentioning that the posterior region of the lateral nucleus (LN) of the amygdala has been recently shown (Chateau and Aron, 1988) to exert an inhibitory control on the display of lordosis behavior in the male rat. On the other hand Ottersen (1982) and Luskin and Price (1983) described intraamygdaloid connections between the LN and the CMN. The possibility then cannot be ruled out that projections to or from the LN may
454
CHATEAU
AND ARON
be involved in the control of lordosis behavior by the CMN in the male rat. A final point is worth noting. It concerns some discrepancy between the effects of the posterior region of the CMN that we observed in the male and those reported by Masco and Carrer (1980) in the female. The reason may be that these authors made smaller lesions in the female than those placed in the male. On the other hand both methodologies differed since Masco and Carrer only took into consideration LQ scores for the evaluation of the sexual receptivity of the female. Previous findings in the female (Al Satli and Aron, 1977) and in the male (Schaeffer and Aron, 1981; Schaeffer et al., 1982, 1986b) have clearly demonstrated that different olfactory mechanisms, involving the main and the accessory olfactory system, are implicated in the regulation of the willingness of both males and females to display lordosis behavior and in the control of sexual performance. The present data then call attention to the necessity of taking into account these two paradigms for the evaluation of lordosis in both sexes. They suggest for the first time the existence of an inhibitory amygdaloid structure that is specifically related to satiety. Indeed, further experiments in the male are required to determine whether peripheral anosmia obtained by instillation of zinc sulfate into the nostrils will induce changes in the sexual performance of ORCH animals primed with gonadal hormones without affecting their willingness to display lordosis behavior. ACKNOWLEDGMENTS We are thankful to Mr. Dujol for the figures and Ms. Gangloff for typing the manuscript. We are indebted to Dr. Roos for the statistical evaluation of the data and to Mr. Weisman for translation verification.
REFERENCES Albe-Fessard, D., Stutinsky, F., and Libouban, S. (1966). Atlas sterPotaxique du dienckphale du rat blanc. Paris, CNRS. At Satli, M., and Aron, Cl. (1977) Influence of olfactory bulb removal on sexual receptivity in the rat. Psychoneuroendocrinology 2, 399-407. Chabli, A., Schaeffer, Ch., Samama, B., and Aron, Cl. (1985). Hormonal control of the perception of the olfactory signals which facilitate lordosis behavior in the male rat. Physiol.
Behav. 35, 729-734.
Chateau, D., and Aron, Cl. (1988). Heterotypic sexual behavior in male rats after lesions in different amygdaloid nuclei. Horm. Behav. 22, 379-387. Chateau, D., Chabli, A., and Aron, Cl. (1987). Effects of ventromedial nucleus lesions on the display of lordosis behavior in the male rat. Interactions with facilitory effects of male urine. Physiol. Behav. 39, 341-345. De Olmos, J., Alheid, G. F., and Beltramino, C. A. (1985). Amygdala. In G. Paxinos (Ed.), The Rat Nervous System, Vol. 1, Forebrain and Midbrain, pp. 223-334. Academic Press, New York. K&rig, J. F. R., and Klippel, R. A. (1963). The Rat Brain. A Stereotuxic Atlas o.f the Forebrain and Lower Parts of the Bruin Stem. Williams & Wilkins, Baltimore.
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Luskin, M. B., and Price, J. L. (1983). The topographic organization of associational fibers of the olfatory system in the rat, including centrifugal fibers to the olfactory bulb. J. Comp. Neurol. 216, 264-291. MacLean, P. D. (1985). Fibers systems of the Forebrain. In G. Paxinos (Ed.), The Rat Nervous System, Vol. 1, Forebrain und Midbrain, pp. 417-440. Academic Press, New York. Masco, D. H., and Carrer, H. F. (1980). Sexual receptivitiy in female rats after lesion or stimulation in different amygdaloid nuclei. Physiol. Behav. 24, 1073-1080. Ottersen, 0. P. (1982). Connections of the amygdala of the rat. IV. Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horse radish peroxydase. J. Comp. Neurol. 205, 30-48. Pfaff, D. W., and Schwartz-Giblin, S. (1988). Cellular mechanisms of female reproductive behaviors. In E. Knobil and J. Neil1 et al. (Eds.), The Physiology of Reproduction, Vol. 2, pp. 1487-1568. Raven Press, New York. Scalia, F., and Winans, S. S. (1975). The differential projections of the olfactory bulb and accessory bulb in mammals. J. Comp. Neuro/. 161, 31-56. Schaeffer, Ch., and Aron, Cl. (1981). Studies on feminine behavior in the male rat: Influence of olfactory stimuli. Horm. Behav. 15, 377-385. Schaeffer, Ch., and Aron, Cl. (1982). Facilitory effects of male urine on feminine behavior in the male rat: Androgen dependency. Physiol. Behav. 29, 677-680. Schaeffer, Ch., Al Satli, M., Kelche, C., and Aron, Cl. (1982). Olfactory environment and lordosis behavior in the female and male rat. In W. Breipohl (Ed), Olfaction and Endocrine Regularion, pp. 115-126. IRL Press, London. Schaeffer, Ch., Chabli, A., and Aron, Cl. (1986a). Endogenous progesterone and lordosis behavior in male rats given estrogen alone. J. Steroid Biochem. 25, 99-102. Schaeffer, Ch., Roos, J., and Aron, Cl. (1986b). Accessory olfactory bulb lesions and lordosis behavior in the male rat feminized with ovarian hormones. Horm. Behav. 20, 118-127. Switzer, R. C., De Olmos, J., and Heimer, L. (1985). Olfactory system. In G. Paxinos (Ed.), The Rat Nervous System, Vol. I, Forebrain and Midbrain, pp. l-36. Academic Press, New York. Winans, S. S., and Scaha, F. (1970). Amygdaloid nucleus new afferent input from the vomeronasal organ. Science 170, 330-332.
AND
BEHAVIOR
23, 448-455 (1989)
Lordosis Behavior in Male Rats after Lesions in Different Regions of the Corticomedial Amygdaloid Nucleus D. CHATEAU ANDCL. Institute
of Histology, Faculty of Medicine, and URA 99 CNRS, Strasbourg,
ARON University Louis Pasteur, 67000, France
The aim of the experiment was to study the effects of stereotaxic lesions of the anterior and the posterior regions of the corticomedial amygdaloid nucleus (CMN) on the display of lordosis behavior by the male rat. Animals were orchidectomized as adults and given estradiol benzoate and progesterone (P) sequentially. Sexual behavior testing was performed by 9 2 1 hr after P injection. Lesions placed into the posterior region of the CMN significantly decreased the proportion of animals showing lordosis behavior as compared to sham-operated and control animals. By contrast lesions in the anterior region of the CMN did not cause any changes in the proportion of animals displaying lordosis but markedly increased the lordosis quotient (LQ) of responding animals. The CMN was then concluded to exert a dual control in the display of lordosis behavior in the male rat with a posterior region regulating the willingness of animals to display lordosis behavior and rostra1 region subserving inhibitory mechanisms related to the sexual performance (LQ values). Q 1989 Academic press. IJK.
Previous experiments in our laboratory (Schaeffer and Aron, 1981; Chabli, Schaeffer, Samama, and Aron, 1985; Schaeffer, Roos, and Aron, 1986b) showed that heterotypic sexual behavior, which is characterized by lordosis responses to male mounts, could be induced in rats orchidectomized as adults and primed with ovarian hormones. Recently Schaeffer er al. (1986) reported that the expression of lordosis behavior in the male rat is regulated in part by the repressive action of the accessory olfactory bulbs (AOB) and Chateau and Aron (1988) showed that the corticomedial amygdaloid nucleus (CMN) exerts in the male rat a facilitatory role in the control of this behavior. This led to the assumption that in the male rat inhibitory mechanisms originating in the AOB were involved in the control of heterotypic behavior by the CMN. It is well known (Winans ans Scalia, 1970; Scalia and Winans, 197.5) that the CMN receives afferent fibers from both the AOB and the main olfactory bulbs (MOB). The former projects to the posteromedial region of the CMN and the latter to the anterolateral region. In the present study, the respective roles played by the anterior and 448 0018-506X/89 $1.50 Copyright All rights
0 1989 by Academic Press, Inc. of reproduction in any form reserved
AMYGDALA
AND
LORDOSIS
IN MALE
RATS
449
the posterior regions of the CMN in the control of heterotypic sexual behavior of the male rat have been investigated. METHODS Animals
Young unexperienced adult male Wistar rats (220-280 g) bred in our colony were used. They were kept under controlled conditions of lighting (lights on 0200-1600 hr) and maintained at a room temperature of 2224°C. They had free access to a commercial laboratory food and tap water. At 3 months of age the animals were orchidectomized (ORCH) under ether anesthesia and then allowed a week postoperative recovery period. Procedure First experiment. The purpose of the first experiment was to examine the effects of lesions of the posterior region of the CMN on the display of lordosis behavior by the male rat. Following orchidectomy bilateral stereotaxic lesions encompassing the traditionally called medial and cortical amygdaloid nuclei were placed into the posterior region of the CMN (Fig. 1B) by passing a cathodic current of 2 mA for 30 set through an epoxylite-coated stainless-steel electrode (diameter 0.25 mm) insulated except for the cut end. Coordinates were AP 4.8; V 1.8; L 3.8 according to Albe-Fessard, Stutinsky, and Libouban (1966). In a group of shamlesioned animals the electrodes were lowered into the brain to a level immediately above the CMN without passing any current. Unoperated animals served as controls. One to 2 weeks after lesioning all the animals received 25 pg estradiol benzoate (EB) in 0.5 ml olive oil subcutaneously (SC) at 1600 hr. They were given 150 pg progesterone (P) 2 days later at 0800 hr and lordosis behavior was tested on the same day between 1600 and 1800 hr. Second experiment. The second experiment was designed to study the effects of lesions of the rostra1 part of the medial and cortical amygdaloid nuclei with limited extension to the basomedial amygdaloid nucleus (Fig. 1A) on the expression of lordosis behavior by the male rat. A week after orchidectomy stereotaxic lesions (2 mA; 30 set) were made using the following coordinates: AP 6.2; V 1.8; L 3.7 (Albe-Fessard et al., 1966). Sham-lesioned animals served as controls. The schedule of sexual behavior testing was the same as in the preceding group. When the experiments were completed, the animals were killed, the brains were fixed in formalin, and the location and extent of the lesions were determined by microscopic examination of frozen unstained serial sections.
450
CHATEAU
AND ARON
FIG. 1. Reconstruction of representative lesions of the anterior part (A) and of the posterior part (B) of the corticomedial amygdaloid nucleus. a, nuclei amygdalae; abl, n. basalis, pars lateralis; abm, n. basalis, pars medialis; ac, n. centralis: ace, n. corticalis; al, n. lateralis; am, n. medialis. The surface of the lesions (striped area) at the plane of maximum size, as seen in unstained serial sections, was drawn on modified stereotaxic plates of Konig and Klippel’s atlas (1963).
Sexual Behavioral
Testing
The lordosis behavior in ORCH rats was tested for 10 min under a dim light in a round 66-cm-diameter mating arena with plastic walls and floor covered with shavings. The ORCH rats were presented to two intact adult sexually vigorous stimulus males (250-350 g) between 1600 and 1800 hr. We selected males that were shown to be fully active when tested at the end of the light period with highly receptive ovariectomized estrogen-progesterone-primed females. They were allowed a 5-min adaptative period in the mating arena prior to the introduction of the ORCH rat. In accordance with previous studies in males primed with ovarian hormones (Schaeffer and Aron, 1981, 1982) we used the following paradigms to evaluate feminine behavior in ORCH rats; (1) the proportion of animals in a given group displaying at least one lordosis response to male mounts; (2) the lordosis quotient (LQ) as computed in each responding animal by dividing the number of lordosis by the number of
AMYGDALA
AND LORDOSIS IN MALE RATS
451
mounts and multiplying by 100. The mean LQ was calculated for each group of responding animals and served as measurement of the mating performance. STATISTICS
The x2 test was used to compare the proportion of ORCH rats displaying lordosis behavior in the different groups of animals. One-way analysis of variance was used for comparing the LQ values (after angular transformation) and the number of mounts by the stimulus males. RESULTS
Effects of Posterior CMN Lesions The results presented in Table 1 show that posterior CMN lesions markedly reduced the proportion of ORCH animals displaying lordosis responses to male mounts with respect to sham-lesioned and intact control animals (x2 = 10.3; P < 0.01; 2 d!. The mean LQ of responding animals did not statistically differ in lesioned, sham-lesioned, and intact control animals (F(2, 22) = 1.89). Neither did the mean number of mounts displayed by the stimulus males differ in these three groups of animals (F(2, 81) = 0.04). Effects of Anterior CMN Lesions As shown in Table 1 rostra1 CMN lesions did not induce any changes in the proportion of animals displaying lordosis responses to male mounts as compared to sham-operated animals (44.1 and 40.5%, respectively; NS). By contrast LQ values of responding animals appeared higher in lesioned (77.5 2 2.6) than in sham-operated animals (48.0 ? 5.7) (F( 1, 30) = 13.41; P < 0.001). The lesioned animals were mounted more frequently by the stimulus males (9.6 t 0.9) than their sham-operated counterparts (7.5 * 0.5) (F(1, 74) = 4.5; P < 0.05). DISCUSSION
Very recently extended lesions of the CMN were shown (Chateau and Aron, 1988) to completely suppress lordosis behavior in ORCH rats primed with gonadal hormones. This led to the assumption that the CMN was absolutely necessary for the male rat to display lordosis behavior. The present study further implicates the posterior region of the CMN in the control of lordosis behavior by the amygdala in the male rat. We observed that lesions located in the posterior region of the medial and cortical amygdaloid nuclei severely impaired the display of lordosis behavior in ORCH rats given 25 pugEB and 150 ,ug P sequentially. The AOB directly projects fibers to the posterior region of the medial and cortical amygdaloid nuclei (Scalia and Winans, 1975; De Olmos,
2sY** 5.7
77.5 + 48.0 f
15/34 I7/42
(44.1%) (40.5%)
31.0 _t 10.5 48.8 k 5.4 40.1 k 4.0
3/32*” ( 9.3%) IO/24 (41.7%) 12/28 (42.8%)
Mean lordosis quotient t SEM in rats displaying at least one lordosis
” All animals received 25 pg EB (SC)at 1600 hr and 150 pg P [SC) 40 hr later. A Testing with two stimulus maIes by 1 to 2 weeks after lesioning and 9 2 I hr after P injection. * P < 0.05 vs sham. ** P c; 0.01 vs sham and controls. *** P < O.OOLvs sham.
_ll----l__.~~~ Experiment I Posterior CMN Iesians Sham lesions Intact controls Experiment z Anterior CMN lesions Sham lesions
Treatment“
Proportion of ORCH rats displaying lordosis ’
9.6 k 0.9* 7.5 i 0.5
9.6 2 0.8 9.9 Ifr 0.9 Y.7 5 0.7
Mean number of mounts -C SEM displayed by the stimulus malt
TABLE I Effects of Lesions of the Anterior and Posterior Regions of’ the Corticomedial Amygdaloid Nucleus (CMN) on Lordosis Behavior in Orchidectomized (ORCH) Rats Primed with Estradiol Benzoatc (EB) and Progesterone (P)
% 2
z
5 2 s
AMYGDALA
AND
LORDOSIS
IN MALE
RATS
453
Alheid, and Beltramino, 1985) which itself projects fibers to the VMN via the stria terminalis (MacLean, 1985). Recently the ABO has been shown to be involved in the mechanisms governing lordosis behavior in the male rat. Schaeffer et al. (1986b) reported that this olfactory structure exerts an inhibitory influence on the display of lordosis behavior in estrogen-progesterone-treated ORCH rats. Additionally, Chateau, Chabli, and Aron (1987) showed that the VMN represents in the male as in the female (for review, see Pfaff and Schwartz-Giblin, 1988) the target for the activation of lordosis behavior by gonadal hormones. All these findings support the view that the facilitatory control exerted by the VMN on lordosis behavior in the male rat is strictly dependent on the CMN which itself is subjected to the inhibitory control of the AOB. However an important question was whether the rostra1 part of the CMN which receives projections from the main olfactory bulb (De Olmos et al., 1985; MacLean, 1985; Switzer, De Olmos, and Heimer, 1985) might be involved in the control of lordosis behavior in the male rat. The present results provided a clear answer to this question. Although the proportion of animals displaying lordosis behavior was not affected by lesions placed in the rostra1 part of the medial and cortical nuclei, LQ values were markedly enhanced in the animals which showed lordosis responses to male mounts. Indeed animals sustaining lesion of the anterior CMN were mounted more frequently than controls. However, we do not believe that this increased mounting contributed the lesions animals’ increased LQ scores. Previous findings in our laboratory (Chabli et al., 1985; Schaeffer, Chabli, and Aron, 1986a) are consistent with this view. Schaeffer, Al Satli, Kelche, and Aron (1982) observed in ORCH rats primed with gonadal hormones a rise in LQ values following anterior olfactory bulb removal disconnecting bulb remnants from nasal passages, thus suggesting that the sexual performance (LQ values) was regulated by the main olfactory system. Therefore it is tempting to suppose that the rostra1 region of the medial and cortical nuclei constitutes the target for the main olfactory system which conveys olfactory cues to the CMN of the amygdala. The CMN then may be considered as a heterogenous nervous structure exerting a dual control on the display of lordosis behavior in the male rat, with a rostra1 region subserving inhibitory mechanisms related to satiety and a posterior region regulating the willingness of animals to display lordosis behavior. It is worth mentioning that the posterior region of the lateral nucleus (LN) of the amygdala has been recently shown (Chateau and Aron, 1988) to exert an inhibitory control on the display of lordosis behavior in the male rat. On the other hand Ottersen (1982) and Luskin and Price (1983) described intraamygdaloid connections between the LN and the CMN. The possibility then cannot be ruled out that projections to or from the LN may
454
CHATEAU
AND ARON
be involved in the control of lordosis behavior by the CMN in the male rat. A final point is worth noting. It concerns some discrepancy between the effects of the posterior region of the CMN that we observed in the male and those reported by Masco and Carrer (1980) in the female. The reason may be that these authors made smaller lesions in the female than those placed in the male. On the other hand both methodologies differed since Masco and Carrer only took into consideration LQ scores for the evaluation of the sexual receptivity of the female. Previous findings in the female (Al Satli and Aron, 1977) and in the male (Schaeffer and Aron, 1981; Schaeffer et al., 1982, 1986b) have clearly demonstrated that different olfactory mechanisms, involving the main and the accessory olfactory system, are implicated in the regulation of the willingness of both males and females to display lordosis behavior and in the control of sexual performance. The present data then call attention to the necessity of taking into account these two paradigms for the evaluation of lordosis in both sexes. They suggest for the first time the existence of an inhibitory amygdaloid structure that is specifically related to satiety. Indeed, further experiments in the male are required to determine whether peripheral anosmia obtained by instillation of zinc sulfate into the nostrils will induce changes in the sexual performance of ORCH animals primed with gonadal hormones without affecting their willingness to display lordosis behavior. ACKNOWLEDGMENTS We are thankful to Mr. Dujol for the figures and Ms. Gangloff for typing the manuscript. We are indebted to Dr. Roos for the statistical evaluation of the data and to Mr. Weisman for translation verification.
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