Benjamin D. Sachs

Functional Analysis of Masculine Copulatory Behavior in the Rat

Publisher Summary This chapter describes the analysis the masculine copulatory behavior of the rat, and focuses over the behavioral elements, the temporal patterning of the elements, and the functional relations among the elements. Many measures of copulatory behavior, initiation latencies, copulatory rate, or number of intromissions, are found to vary rather independently of each other, and this evidence is taken as support for the view that sexual arousal is not unitary. The chapter explains how this functional analysis speaks to some of the models that have been developed. The data presented in the chapter explains that some or all of the arousal systems have inhibitory counterparts. This is particularly clear with respect to the absolute and relative post-ejaculatory refractory periods, but probably it is also true of systems controlling behavior prior to ejaculation. The evidence that the number of intromissions needed for ejaculation is substantially independent of the speed of this copulatory clock is also addressed. The chapter relates the behavioral analysis to a number of theoretical models of copulatory behavior. The primary concern in this chapter is to describe how the elements of copulatory behavior are wired together, rather than how the nervous system controlling that behavior is wired together. Nevertheless, behavioral and physiological analysis must proceed in parallel, and the consideration of the physiological evidence reminds us forcefully how little is known about the physiological mechanisms underlying sexual behavior.

Copulatory behavior in male rats with lesions in the bed nucleus of the stria terminalis.

Abstract Male rats receiving lesions in the bed nucleus of the stria terminalis(BNST) displayed more intromissions preceding each of three ejaculations in a test. BNST-lesion males also tended to be slower in the temporal patterning of copulation. The present data, together with recent reports of corticomedial amygdala modulation of copulation, indicate an involvement of the amygdala-strial system in the achievement of ejaculation and, to a lesser degree, in the temporal aspects of copulation.

RORα coordinates reciprocal signaling in cerebellar development through Sonic hedgehog and calcium-dependent pathways

The cerebellum provides an excellent system for understanding how afferent and target neurons coordinate sequential intercellular signals and cell-autonomous genetic programs in development. Mutations in the orphan nuclear receptor RORalpha block Purkinje cell differentiation with a secondary loss of afferent granule cells. We show that early transcriptional targets of RORalpha include both mitogenic signals for afferent progenitors and signal transduction genes required to process their subsequent synaptic input. RORalpha acts through recruitment of gene-specific sets of transcriptional cofactors, including beta-catenin, p300, and Tip60, but appears independent of CBP. One target promoter is Sonic hedgehog, and recombinant Sonic hedgehog restores granule precursor proliferation in RORalpha-deficient cerebellum. Our results suggest a link between RORalpha and beta-catenin pathways, confirm that a nuclear receptor employs distinct coactivator complexes at different target genes, and provide a logic for early RORalpha expression in coordinating expression of genes required for reciprocal signals in cerebellar development.

Electromyographic analysis of male rat perineal muscles during copulation and reflexive erections

Anatomical examination of the ventral bulbospongiosus (BS) muscle suggested that its proximal and distal portions may act during penile erection as a two-stage pump governing the intensity of glans erections. The coordination between these portions of the BS, and of the proximal BS with the ischiocavernosus (IC) muscle, was studied using electromyographic (EMG) recordings taken during copulation and reflexive erections. Mounts without intromission were accompanied by either strong IC activity with little or no proximal BS activity, or strong proximal BS activity preceding the onset of IC activity. Activity in the proximal BS during mounts was variable in both duration and amplitude but uniform in frequency. During mounts with intromission, EMG activity of the proximal BS consisted of two characteristic phases, an early phase of low-amplitude activity which was similar to proximal BS activity during nonintromissive mounts, followed by an intromissive phase of high-amplitude, high-frequency activity. During intromission patterns, IC activity reliably preceded proximal BS activity. Ejaculations were accompanied by stronger proximal BS activity than were other copulatory events and were followed by a series of proximal BS and IC bursts lasting for 10-20 seconds. During reflexive erections, EMG activity in the proximal BS was always fusiform and varied with the intensity of erection only in frequency. In contrast to the proximal BS, activity in the distal BS was similar in frequency and amplitude across copulatory and reflexive events. These findings suggest that: a) different motoneuron pools serve the different portions of the BS muscle; b) the distal BS does not differentially affect glans erection but may serve primarily to promote rigidity of the portion of the bulb that it surrounds, while the proximal BS acts as the variable aspect of a hypothetical two-stage pump, and c) activity in the IC must precede activity in the proximal BS to achieve intromission.

Noncontact stimulation from estrous females evokes penile erection in rats

Five experiments demonstrated that noncontact stimulation from estrous females evokes penile erection in a high proportion of sexually experienced male rats. In Experiment 1, 23 of 24 males (96%) displayed erections while separated from estrous females by a wire-mesh barrier, compared with 8% when no female was present. In Experiment 2, inaccessible estrous females stimulated erection in 100% of males, whereas only 38% responded to inaccessible unfamiliar males and 0% to inaccessible preferred food or an empty cage (n = 8/group). These data suggest that nonsexual arousing stimuli do not readily evoke erections. Experiments 3 and 4 demonstrated that bedding collected from estrous females is highly attractive to males, but is ineffective in promoting erections even when the males can burrow in the bedding. Therefore, estrous odors alone are apparently insufficient to stimulate erection. In Experiment 5, the percentage of males (n = 18) responding with erection did not vary significantly as a function of their exposure to ovariectomized females (67%), receptive but nonproceptive females (83%), or proceptive females (89%), but these stimuli were progressively more effective in reducing erection latency and increasing the number of erections displayed, suggesting that behavioral cues emitted by females promote erection. The display of erection by rats under the conditions used in these studies satisfies conventional criteria for recognition as psychogenic erections, which we have provisionally defined as erections that occur without concurrent somesthetic stimulation. The availability of a rodent model of psychogenic erection should foster analysis of its physiological mediation.

Erection Evoked in Male Rats by Airborne Scent from Estrous Females

In the presence of inaccessible estrous females, male rats display penile erections and associated stereotypic behavior indicative of sexual arousal. The effective stimuli for these noncontact erections (NCEs) had not been determined, but bedding soiled by estrous females was known to be ineffective. The present experiments tested for a potential role for volatile olfactory cues in evoking NCE. In Experiment 1, sexually naive male rats were observed for NCEs when tested with inaccessible, estrous females, upwind (n = 20) or downwind (n = 20) from them under conditions that permitted or prevented visual communication. After half the males in each condition had copulatory experience, they were tested under the same conditions. In each test, only on male of 20 responded with females downwind, whereas about half the 20 males displayed NCEs with females upwind, irrespective of barrier type or, in Test 2, of sexual experience. Olfactory cues from estrous females were apparently necessary to induce NCE, whereas visual and auditory stimuli from estrous were not sufficient to evoke NCE, nor did they affect the response to olfactory stimulation. In Experiment 2, males were downwind from estrous females (n = 10) or anestrous females (n = 10) that were behind opaque barriers and were anesthetized to preclude auditory communication. Results indicated that olfactory cues were also sufficient to provoke NCE in sexually experienced males. Receptive female rats apparently broadcast a volatile pheromone that promotes erection. Pheromones are well known to attract potential mates and to act in concert with other stimuli to promote mating. However, this is the first mammalian evidence for a volatile pheromone acting alone to evoke a sexual fixed-action pattern and, in that sense, acting as an airborne aphrodisiac.

Penile reflexes and copulatory behavior in male rats following lesions in the bed nucleus of the stria terminalis.

Male rats with large lesions in the bed nucleus of the stria terminalis (BNST) had more intromissions preceding ejaculation (if they ejaculated at all), longer intervals between intromissions, and longer postejaculatory refractory periods than control animals. In tests for penile reflexes, BNST males were similar to control males in every respect. The copulatory deficits in BNST males are probably not mediated by a change in penile reflex potential.

Conceptual and Neural Mechanisms of Masculine Copulatory Behavior

This chapter deals with the conceptualization of masculine copulatory behavior in mammals, and with the search for the neural basis of this behavior. My thesis, in part, is that the search for the central neural control of sexual behavior has not led to the dicoveries and sense of understanding that many expected when the search began. The relatively slow rate of progress stems partly from the apparent complexity of the neural control, and from the technical difficulties in tracing that control. The difficulties in understanding the neural control might have been more easily anticipated, though perhaps not avoided, had there been greater concurrent conceptual analysis of the behavior patterns.

Importance of the medial amygdala in rat penile erection evoked by remote stimuli from estrous females.

Effects of medial amygdala lesions (MAL) were examined on rat penile erection in three different experimental situations. Only sexually vigorous males, as identified by preoperative mating tests, were used. Bilateral radiofrequency lesions were confined to the posterior medial amygdala, with little systematic damage to anterior medial amygdala or to adjacent structures. Lesion electrodes were withdrawn without current application in sham-operated animals (SHAM). After recovery for brain surgery, males were tested for (1) noncontact erection (NCE) that occurs when males were placed in proximity to inaccessible estrous females, (2) reflexive erection evoked in supine males by retraction of the penile sheath, and (3) copulatory behaviour with receptive females. In the NCE test, none of the MAL males showed penile erection during the 20 min observation, whereas 70% of the SHAM males showed it (P < 0.001). In contrast, no erectile dysfunction in the MAL males was detected in the other two tests. MAL males displayed more penile-body erections (flips) than SHAM males in the reflexive-erection test (P <0.05). In the copulation test, most of the MAL males achieved intromission, but their intromission ratio, a partial measure of erectile function, was marginally lower than that of SHAM males (P = 0.051). MAL males had longer intervals between intromissions (P < 0.001); as a result, none of them ejaculated during the 30 min period that followed the first intromission. The results suggest that the posterior medial amygdala plays an essential role in the regulation of NCE, and it may also contribute to the regulation of erection in other contexts.

Grooming in Norway Rats: the Development and Adult Expression of a Complex Motor Pattern

In two experiments detailed observations and quantitative analyses were made of the development and adult expression of grooming in laboratory rats. In the first experiment, 5 litters of rat pups were observed each day from 0-28 days of age, and grooming movements were recorded on paper. Forepaw wipes of the nose appeared by Day 3, followed by eye wipes (Day 6) and ear wipes (Day 8). These movements were integrated into normal-appearing head grooming on Day 11. The mouth was used to groom posterior portions of the body beginning on Day 14 with the belly, and continuing subsequently with hip (Day 15), back (Day 18), and the anogenital region and tail (Day 20). Thus, these aspects of grooming followed a general cephalocaudal progression. In contrast, the development of scratching of the head and body, which began on Day 6, did not follow a systematic order. In the second experiment, 5 adult male rats were observed in glass aquaria, which also served as their living compartments, and bouts of grooming were recorded on videotape for later analysis. Sequential and spatial characteristics of movements were determined by replaying the videotapes in slow motion, while temporal characteristics were determined by a frame-by-frarne analysis of the tapes. This experiment revealed a cephalocaudal progression of acts within bouts of grooming: grooming usually began with the paw-lick- nose-wipe sequence and progressed from there to eye wipes and ear wipes. Mouthing of the torso followed, usually beginning with more anterior portions and terminating with more posterior portions. Scratching with the hindpaws was unpredictably interpolated into the grooming sequence. The experiment also revealed that transitions between grooming different parts of the body were predictable from the spatial and temporal characteristics of the grooming. That is, the last stroke in chains of nose, eye, or ear wipes was reliably slower than previous strokes in the chain, and also tended to be incomplete. Thus, the order in which grooming of specific body areas emerges during early development follows an anterior-posterior progression, and this progression closely parallels the sequence in which body areas are groomed by adult rats. Furthermore, in adults these movements obey specific temporal and spatial rules which can be used to predict transitions of grooming from one body area to the next. This parallel between the ontogenetic and adult expressions of grooming may reflect, respectively, the maturation and activation of genotypically determined, functional units in the central nervous system. In addition, theories now being applied to the problem of transitions between different motive systems (e.g., eating and drinking), may be extended to account for transitions within a motive system (e.g., from grooming of one part of the body to the next).