Estrous Changes in Responses of Rat Gracile Nucleus Neurons to Stimulation of Skin and Pelvic Viscera

Abstract

Multi-and single-unit recording was performed in the gracile nucleus in urethane-anesthetized rats to examine estrous variations in responses of its neurons to brushing the hindquarters and mechanical stimulation of the uterus, vaginal canal, cervix, and colon. Six rats each were studied in each of the four estrous stages: proestrus (P), estrus (E), metestrus (M), and diestrus (D). The magnitude of multi-unit responses to gentle brushing of the perineum, hip, and tail, but not the foot and leg, was significantly greater during proestrus than during other stages. Of 70 single units responsive to brush, 56 (80%) responded to stimulation of at least one viscus. Although this percentage did not change with estrous stage, the direction and latency of some responses did. Pressure on the cervix evoked significantly more inhibitory (vs excitatory) responses in P than in E and M, and the response latency was significantly longer in D and P than in E and M. The direction of response to vaginal distention did not change with estrous stage, but response latency was significantly longer in D than in P and E. Uterine distention evoked significantly more inhibitory responses in D than in P, with no estrous changes in latency. Responses to colon distention did not change. These variations in both magnitude of response to tactile stimulation and characteristics of response to stimulation of reproductive organs, but not the colon, correlate with changes in mating behaviors of the female rat, suggesting that the gracile nucleus is a component of neural systems that control reproductive behaviors.Key words: female; dorsal column; reproduction; plasticity; somatosensory; pain It is well known that neurons in the gracile nucleus (NG) receive input from low-threshold cutaneous primary afferent fibers, respond vigorously to gentle tactile stimulation of small areas of the hindquarters, and convey that information to the thalamus and somatosensory regions of the cerebral cortex. It has been found recently, however, that NG neurons in the rat also respond to innocuous and noxious stimulation of female pelvic organs, such as the cervix, uterus, vagina, and colon (Hubscher, 1994;Berkley and Hubscher, 1995).Such convergent responsiveness suggests that NG may be a component of neural systems that coordinate reproductive behaviors. These behaviors in the female rat include a group of complex pacing and darting movements collectively called "proceptive behaviors," which are important for successful mating (Erskine, 1989), as well as "lordosis," which is a mating posture important for copulation and successful fertilization (Schwartz-Giblin et al., 1989;Pfaff, 1997). Both behaviors vary with the rat's estrous cycle in a similar way. Proceptive behaviors occur during the female rat's fertile period when she is sexually receptive, that is, during the afternoon and evening of proestrus and during the early morning of estrus (Erskine, 1989). This period is when estrogen and progesterone rise and fall in conjunction with ovulation (Freeman, 1994). L...

Cross-organ interactions between reproductive, gastrointestinal, and urinary tracts: modulation by estrous stage and involvement of the hypogastric nerve

“…Furthermore, given earlier findings suggesting that crossorgan effects could be influenced by reproductive status (15,16,18), we also tested the hypothesis that any cross-organ effects observed in this study would vary by estrous stage.…”

“…Studies have shown, however, that neurons in the spinal cord, dorsal column nuclei, solitary nucleus, medullary reticular formation, and thalamus process information that converges from different internal organs located in different functional systems, i.e., the reproductive, gastrointestinal, and urinary tracts (8,9,11,17,24,31,32,37,57,58,59,60). In some regions, this processing is robustly influenced by the estrous cycle and hormone manipulations (15,16).This cross-system, viscerovisceral convergence supports the concept that the nervous system provides a dynamic substrate [whose characteristics are modified by reproductive status (47)] that permits events occurring in one organ to influence functioning of other organs. Influences like these are clearly important during healthy events, such as parturition, as well as more common functions, like those occurring during coitus, urination, and defecation, which normally are mutually inhibitory (7,27,28,34,49,60,63).…”

“…Studies have shown, however, that neurons in the spinal cord, dorsal column nuclei, solitary nucleus, medullary reticular formation, and thalamus process information that converges from different internal organs located in different functional systems, i.e., the reproductive, gastrointestinal, and urinary tracts (8,9,11,17,24,31,32,37,57,58,59,60). In some regions, this processing is robustly influenced by the estrous cycle and hormone manipulations (15,16).…”

17- -Estradiol Enhanced Allodynia of Inflammatory Temporomandibular Joint through Upregulation of Hippocampal TRPV1 in Ovariectomized Rats

“…Although animal studies showed that estradiol can attenuate pain (Gaumond et al, 2005;Kuba et al, 2006;Mannino et al, 2007) or has no effect (Mannino et al, 2005), there are also comparable animal studies that argue that estradiol exacerbates peripheral pain sensitization by decreasing mechanical threshold or increasing response to noxious stimuli administered to the colon and vagina (Bradshaw and Berkley, 2000;Evrard and Balthazart, 2004). Despite the controversy, we showed here that estradiol could exacerbate mechanical allodynia of inflamed TMJ in the ovariectomized rats, suggesting that rats with a higher level of plasma estradiol would be more sensitive to mechanical stimuli over the inflamed TMJ.…”

Rapid Regulation of Pain by Estrogens Synthesized in Spinal Dorsal Horn Neurons

“…The hormone 17␤-estradiol (E2) regulates a remarkably large spectrum of neural functions, including nociception (Amandusson et al, 1999;Bradshaw and Berkley, 2000;Liu and Gintzler, 2000;Ji et al, 2003). The effects of E2 in neurons primarily rely on intracellular nuclear receptors [estrogen receptor ␣ (ER␣) and ER␤] controlling gene transcription and impacting physiology and behavior within hours to days (Jensen and DeSombre, 1973;Paech et al, 1996).…”