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Disparate effects of small medial amygdala lesions on noncontact erection, copulation, and partner preference

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Abstract

Male rats with radiofrequency lesions in the anterior medial amygdala (MeAa) or the posterior medial amygdala (MeAp), respectively, were tested for copulation and for noncontact erection (NCE; evoked by inaccessible estrous females) in a chamber in which the male was located between estrous and anestrous females. Barriers allowed only olfactory and auditory interaction between animals. With conscious females as stimuli, MeAp lesions virtually eliminated NCEs, and MeAa lesions moderately impaired them, without affecting the normal preference for estrous over anestrous females. When tested with anesthetized females to remove auditory stimulation, few males with lesions had NCEs. Only the males with MeAp lesions had a significant reduction in preference for estrous over anestrous anesthetized females. Neither MeAa nor MeAp lesions had an effect on copulatory behavior. MeAp lesions may have caused a reduced sensitivity to—or impaired processing of—estrous odors, thereby preventing NCE without disrupting copulatory behavior.

Introduction

The importance of the medial amygdala (MeA) for normal male sexual behavior has been well established by convergent evidence. Lesions of the MeA impair this behavior [7], [9], [13], [16], [17], and hormones delivered to the MeA can restore mating behavior in castrated male rats [2]. Also, the MeA is active during sociosexual encounters, as reflected by neurophysiological recording [28] and by increased presence of early-immediate gene products such as Fos [1], [3], [10], [11], [12], [14], [21], [23], [30]. The Fos research has enabled greater specificity in identifying areas of the MeA that are important for copulatory behavior and the functional roles of those areas. The lateral margin of the posterodorsal MeA (MeApd) of rats shows Fos expression after one or more ejaculations but not after lesser amounts of copulation [5], [6]. Conversely, more medial portions of MeApd express Fos after lesser amounts of sociosexual stimulation, including exposure to the odors of estrous females [6].

Some of the early studies implicating MeA in copulation in rats used lesions so large that they included both cortical and MeA and were identified as ‘corticomedial amygdala’ [9], [13]. In sexually inexperienced rats, lesions restricted to the MeA prevented copulation, not just ejaculation [16]. However, the nature of the deficit resulting from these lesions remains unresolved.

MeA lesions in rats were recently found to impair not only copulation, but also noncontact erection (NCE), i.e. the erectile response to inaccessible estrous females [17]. In that study, lesions were limited to the posterior MeA (MeAp), precluding conclusions about a role for the anterior MeA (MeAa) in NCE. Therefore, in the present study, we compared effects of MeAa and MeAp lesions on NCE. Also, no attempt had been made to analyze the origins of the deficit in NCE. For example, the MeA receives major projections from the olfactory bulbs [29], and the lesioned males may have failed to process the olfactory stimuli that are sufficient to evoke erection [19], [26]. However, the studies did not exclude the possible role of auditory stimuli. In the present study, we also tested MeA lesioned males for preference and NCE using females made silent by anesthesia, leaving only olfactory stimuli from the female available to the male.

Section snippets

Materials and methods

Eighty-three male Long–Evans hooded rats (BLU, Harlan Sprague Dawley, Indianapolis, IN; 2 months old upon arrival) formed the pool from which 51 rats were selected on the basis of behavioral screening. Female rats of the same strain served as mating partners or stimuli for the NCE/preference tests. The two sexes were kept in different rooms under the same conditions of illumination (lights on 23:00–11:00), and room temperature (23±2 °C). Males selected as subjects had reached the first

Location of lesions

We reassigned animals in accordance with the histological verification of lesions, which were relatively small. Accordingly, rats not in the Sham group were reassigned as follows: lesion restricted to the MeAa (ANTx, n=11), lesion restricted to the MeAp (POSTx, n=7), and misplaced or incomplete lesions (MISx, n=13). Six animals were not included because their lesions were located between the MeAa and the MeAp. (Data from these males are available upon request.) Fig. 1 shows the lesion areas

Discussion

These data confirm previous findings that small lesions in the MeAp profoundly impair NCE [17], and they indicate that MeAa lesions cause a lesser impairment in NCE. The treatment groups did not differ in their preference for conscious receptive females, with which olfactory and auditory communication was possible. When auditory communication was prevented by anesthetizing the females, only MeAp lesions significantly decreased %TimeNPE compared to that with conscious females. The lesions had no

Acknowledgements

We thank Philip G. Jordan for his excellent assistance in this research, which was supported by NSF research grant IBN-9603917.

References (30)

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