Covergent effects of lordosis-relevant somatosensory and hypothalamic influences on central gray cells in the rat mesencephalon.
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Publications and source records attributed to D W Pfaff.
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1. To analyze further the sensory mechanisms for triggering the lordosis reflex, single-unit (n = 345) activity was recorded extracellularly from spinal segments L5-S1 of urethan-anesthetized female rats. Unit responses to pressure on the skin (necessary and sufficient for evoking lordosis) and other mechanical stimuli were studied. 2. Units were classified according to their responses to the battery of mechanical stimuli: 16% of the units responded only to pressure. The majority of these pressure-responsive units were excited, while a few were inhibited or responded differently, depending on the site stimulated; 52% did not respond to pressure, but responded to brushing, muscle-joint, and/or visceral stimulation, or did not respond at all. The remaining 32% responded to pressure plus other forms of stimulation. 3. Units responding only to the movement of individual types of hair tended to be located in the dorsal horn, more dorsal than units responding only to pressure (found primarily in the intermediate gray). Units responding to subdermal stimulation were usually found at greater depths. Segmental and somatotopic distributions of spinal units observed were very similar to those reported for cat (3) and monkey (5). 4. Compared to primary sensory units (28), spinal units had higher resting firing rates, more complicated responses to a given stimulus, a wider variety of unit types, and much larger receptive fields. These comparisons tend to indicate convergence of primary sensory neurons onto individual spinal units. 5. The range of pressure thresholds of pressure-responsive units is comparable to the range effective for triggering lordosis. We postulate that excitation of units responding only to pressure is centrally involved in triggering the lordosis reflex. Those units not responding to pressure are probably irrelevant for this behavior. Presently undetermined are the roles of units with complex or mixed-response types.
1. Seventy-four neurons in the central gray of the mesencephalon were antidromically activated by electrical stimulation of the gigantocellular and magnocellular nuclei region of the ipsilateral medullary reticular formation in urethan-anesthetized female rats. An additional eight cells were located contralaterally. With control of the lordosis reflex (facilitated from central gray) in mind, each cell was characterized by the properties of its antidromic response and by its response to pressure stimulation of the hindquarters of the hindquarters of the animal. 2. The antidromically activated spikes had constant latencies between 1.0 and 25.5 ms, with a mean of 10.7 +/- 0.7 ms. 3. Cells of origin of the descending projections were located in all parts of the central gray and adjacent mesencephalic reticular field except within the inner ring of the central gray that surrounds the cerebral aqueduct. A particularly dense group of cells was noted in the ventrolateral aspect of the central gray. Fewer were found in the dorsal central gray over the cerebral aqueduct. 4. These cells had very low rates of spontaneous discharge or none at all. No specific changes in activity could be elicited by lordosis-relevant somatosensory stimuli. Therefore, these cells appear not to be involved in stimulus-bound reflexive control of lordosis behavior. Instead, they may be engaged in mediating influences descending from hypothalamus, known to control lordosis (see Ref. 48). In turn, they could modulate activity in reflex arcs completed at lower levels of the neuraxis.
1. Effects of estrogen on the excitability of 74 neurons in the central gray of the mesencephalon (CG) antidromically identified from the medulla were investigated extracellularly in female rats under urethan anesthesia. 2. The mean rate of spontaneous discharge of the identified CG cells was higher in estrogen-treated (2.9 Hz) than in untreated ovariectomized rats (0.3 Hz). In the estrogen-treated preparations, 18.5% of the identified cells had discharge rates exceeding 3.0 Hz, while none were found in this range in the untreated animals. 3. Two types of positive-negative biphasic antidromic spike potentials were distinguished. In one ("fast") the initial positive deflection was completed within 500-700 microseconds, while it took longer than 1 ms in the other ("slow" spikes). Slow spikes had a notch in the rising phase of their initial positive deflection, at which antidromic propagation was often blocked. Mean antidromic spike latency for the fast spikes was 6.8 ms, while the value for the slow spikes was 14.7 ms. 4. In slow spikes, the percentage of successful antidromic spike invasions into the somatodendritic complex remained constant for a long time when the response was elicited by repetitive antidromic stimuli at 0.5 Hz. Antidromic propagation into the somatodendritic complex occurred more frequently in the slow spikes recorded from estrogen-treated preparations (94.2%) than in those of ovariectomized untreated animals (55.7%). 5. Electrical stimulation of the preoptic area (POA) reduced the frequency of successful antidromic propagation into the somatodendritic complex. Stimulation of the ventromedial nucleus of the hypothalamus (VMN) increased it. Conversely, electrolytic lesion of the POA facilitated, while VMN lesion reduced antidromic spike invasion. 6. Thus, excitability of some neurons in the CG is facilitated by estrogen. Similar effects of VMN stimulation and POA lesion suggest that the estrogenic effect could be mediated by these structures. The pattern of effects on these CG neurons is that required for their control of lordosis behavior, an estrogen-dependent postural reflex in female rodents. These cells may modulate medullary reticulospinal cells, which in turn govern the reflex.
The dorsal and ventral vertebral muscles of the back and the tail of the albino Norway rat are described and discussed. These muscles were analyzed because they are undoubtably used during the sexual posturing, lordosis, of the female rat, as well as participating in a variety of other behaviors. The muscles are described by region (thoracic-lumbar or sacrocaudal), and the classifications of Vallois are followed where possible. Of the epaxial (dorsal) muscles, the three longitudinal systems of muscles, the transversospinalis, the longissimus, and the iliocostalis systems, can be identified in the albino rat. Muscles of the transversospinalis system are fused in the lumbar region, distinct and specialized in the thoracic region, and form the tail muscle extensor caudae medialis caudally. The iliocostalis system of the lumbar region is fused with one component of the lumbar longissimus system to form lateral longissimus. Anteriorly, iliocostalis thoracis and cervicis represent the iliocostalis system. The lumbar longissimus system is represented by the longissimus component of lateral longissimus, medial longissimus, and a short-fiber component. Longissimus dorsi is the anterior continuation of the longissimus portion of the lateral longissimus. The short-fiber component also continues into the thoracic region, where it becomes difficult to separate out from longissimus dorsi. Medial longissimus represents the excursion into the lumbar region of the long, tendinous, tailbase-tail muscle, longissimus caudae; the caudal portion of this muscle is extensor caudae lateralis. The remaining dorsal muscle described is the tail muscle, abductor caudae dorsalis. The hyposomal (ventral) muscles described are quadratus lumborum and the intertransversarii, present in the lumbar region; the muslces iliococcygeus, pubococcygeus and coccygeus which arise from the medial face of the pelvis and insert onto the proximal tail; the long, tendinous, tail muscles, flexor caudae brevis and longus; and the ventral and lateral set of segmental tail muscles. The innervation of the lumbar transversospinalis muscles by the medial branches and of lateral longissimus by the lateral branches of the dorsal rami of the spinal nerves was traced and confirmed by electrical stimulation of the nerve branches. The innervation of medial longissimus is also described. Additionally, movements of the vertebral column produced by direct unilateral or bilateral muscle stimulation were observed for a number of the muscles.
Ablations of lateral longissimus, medial longissimus, and the lumbar transversospinalis system were performed singly and sequentially on female albino rats. Animals were tested postoperatively with males and by manual stimulation for lordosis. In tests with males, the strength of lordosis was rated specifically with respect to the extent of rump elevation; in manual stimulation tests, rating was based on the full lordotic response. Animals were also tested for the ability to cross a balance beam as an indication of the general status of the animals' posture and locomotion. The data from tests with males proved more sensitive in showing up effects of the ablations on lordosis. Lateral longissimus ablations and transversospinalis ablations led predictably to worsened lordosis. Medial longissimus ablations did not significantly affect lordosis. The manual stimulation data were consistent with the data obtained in tests with males. Ablated animals were not impaired on the balance beam test. The results indicate that lateral longissimus and the lumbar transversospinalis system are major participants in the rump elevation of lordosis, an early and biologically important component of the lordotic response. This information permits focus on lateral longissimus and the lumbar transversospinalis system in the investigation of the neural control of lordosis.
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The presence and the neuroanatomical topography of sex hormone concentrating cells in the brain of the American chameleon, Anolis carolinensis have been demonstrated by these experiments. After 3H-estradiol administration large numbers of hormone concentrating cells were found in the amygdala, septum, medial preoptic area, anterior hypothalamic area, the ventromedial and periventricular nuclei of the hypothalamus, and anterior pituitary. In addition, labelled cells were found in the torus semicircularis, in and around the nucleus isthmus pars parvocellularis. A small number of labelled cells could also be found in the rostral pallium, motor nucleus of the fifth cranial nerve, the raphé nuclei, and the spinal cord. After 3H-testosterone or 3H-dihydrotestosterone administration the neuroanatomical pattern was very similar to that found after 3H-estradiol; however, fewer labelled cells were seen after the androgens were given. Two exceptions to the similarity of pattern were in a caudal part of the pallium and in the mesencephalic tegmental area. Hormone-concentrating cells were found after 3H-testosterone or 3H-dihydrotestosterone administration, while labelled cells in these two areas after 3H-estradiol administration were extremely rare. The pattern of hormone-concentrating cells was the same in male and female brains, for each of the hormones. The preoptic area, hypothalamus, and anterior pituitary have been demonstrated in reptiles to be involved in neuroendocrine regulation and in the control of sex behaviors. The presence and neuroanatomical pattern of sex steroid binding cells in the brains of a wide variety of vertebrates have been documented. Large numbers of hormone-concentrating cells were found in all of these species in the medial preoptic area, tuberal hypothalamus, specific limbic structures, the mesencephalon deep to the tectum, and the anterior pituitary. Most hormone-concentrating cells in the brain of A. carolinensis were found in these same brain regions, thus indicating a vertebrate-wide stable core of hormone-concentrating cells in neuroanatomically defined regions.
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In the rat, lateral longissimus and the lumbar transverso-spinalis muscles are lumbar trunk muscles, and participate in the lordosis reflex (female sexual posturing). Medial longissimus, the remaining major lumbar epaxial muscle, is a muscle of the proximal tail-tailbase. To allow an analysis of the motor control of lordosis, motoneurons for these muscles must be localized. Horseradish peroxidase (HRP) was injected into lumbar epaxial muscles of female rats. Following injection into medial longissimus, labeled cells were found posterior to the lumbar enlargement, ventrolaterally in the ventral horn. Following injections into lateral longissimus or into lumbar transverso-spinalis muscles, most labeled cells were found on the medial side of the ventral horn, extending through and anterior to the lumbar enlargement. Injections into lumbar transverso-spinalis muscles at more posterior levels led to more posterior locations of labeled cells. The distributions of the labeled cells agree with previous observations on innervation of the muscles. Additionally, the spinal cord was scanned for sites at which microstimulation produced visible twitches of medial longissimus or transverso-spinalis muscles. Locations of low threshold twitch sites were consistent with conclusions based on the HRP findings.
Efferent projections from the ventromedial nucleus of the hypothalamus (VMN) were traced using tritiated amino acid autoradiography in albino rats. Ascending fibers passed through the anterior hypothalamus. Labelled fibers and terminal fields were seen in the preoptic area, bed nucleus of the stria terminalis, substantia innominata, the anterior amygdaloid area, diagonal bands of Broca and lateral septum. Fibers also projected laterally from VMN and entered the supraoptic commissures and zona incerta. These lateral projections were responsible for the fibers observed in the cerebral peduncle, the amygdala, the thalamus and the reticular formation. Fibers descending in a medial position projected through the posterior hypothalamus and then swept dorsally to terminate in the mesencephalic and pontine central grey. A projection from VMN into the median eminence was noted. The overall patterns of projection from different parts of VMN were similar; differences that existed were primarily in the relative strengths of the different projections. The efferent projections from VMN are extensive, well organized, and would appear capable of supporting significant physiological actions on extra-hypothalamic structures.
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Electrical stimulation in the mesencephalic central gray (CG) and adjacent subtectum through chronically implanted electrodes in free-moving estrogen-primed ovariectomized female rats elicited a rapid and large facilitation of the lordosis reflex in response to either male mounts or manula cutaneous stimuli. Unilateral stimulation was sufficient for this effect. The facilitation increased in a graded manner to increased stimulus intensity, and was optimally evoked by stimuli delivered at 50--150 Hz. Facilitation disappeared rapidly following the end ot electrical stimulation, and within 15 min, reflex performance returned to the prestimulation level. Lordosis facilitation appeared when no aversive responses occurred; stimulation with comparable parameters at the lateral edge of CG or in the mesencephalic reticular formation often resulted in postural changes or aversive responses but was not able to facilitate lordosis. Lordosis refelx facilitation was probably mediated by projections descending from neurons in and around the CG, and represents stimulation of a functional link between ascending somatosensory and descending motor systems for the control of lordosis behavior.
Placement of bilateral electrolytic lesions in the mesencephalic central gray (CG) of estrogen-primed ovariectomized female rats produced an immediate decline in performance of the lordosis reflex. Lesions that destroyed the dorsal half of the CG and the adjacent subtectal region were effective. The decrease in individual animals in terms of the lordosis reflex score ranged from 20 to 100% of the prelesion performance. Such lesions abolished the facilitation of lordosis by electrical stimulation of the ventromedial nucleus of the hypothalamus. Similar abrupt losses of lordosis followed bilateral lesions of either a) the area between CG and the cuneiform nucleus of the mesencephalic reticular formation (NCf); or b) the ventrolateral quadrant of the NCf. The difference between these two lesions was that the effect of the latter could be overridden by electrical stimulation of the CG, whereas that of the former could not. We conclude that the CG is an important supraspinal component of the circuit for lordosis behavior, constituting a link between ascending somatosensory and descending motor systems for lordosis. It probably facilitates lordosis when activated by behaviorally relevant peripheral somatosensory and/or ventromedial hypothalamic inputs.