Estrous cycle variation of afferent fibers supplying reproductive organs in the female rat

Robins, Ann; Berkley, Karen J.; Sato, Yuko

doi:10.1016/0006-8993(92)91572-v

Cited by 91 publications

(48 citation statements)

References 19 publications

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“…Although there are estrous changes in vaginal structure and physiology (Long and Evans, 1922), as well as in response properties of vaginal afferents (Robbins et al, 1992), the major vaginal changes occur between proestrus/estrus and metestrus/ diestrus. Thus, vaginal changes across the estrous cycle do not parallel behavioral changes, which occur between proestrus and estrus (Cason et al, 2003).…”

Section: Mechanisms Of Endo-induced Versus Ovx-induced Vaginal Hyperamentioning

confidence: 99%

Endometriosis-induced vaginal hyperalgesia in the rat: Effect of estropause, ovariectomy, and estradiol replacement

Berkley

McAllister

Accius

et al. 2007

Pain

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Endometriosis (ENDO) is a painful disorder defined by extrauteral endometrial growths. It is created in rats by autotransplanting pieces of uterus (which form cysts), or, for shamENDO, fat (no cysts). ENDO induces vaginal hyperalgesia, likely via central sensitization. The severity of this hyperalgesia correlates with estradiol levels during the estrous cycle, suggesting the hyperalgesia is estradiolmodulated. If so, then hyperalgesic severity should track estradiol changes during reproductive senescence (estropause) when estradiol levels initially decrease, then increase. Using psychophysical methods to assess vaginal nociception, we found that the severity of ENDO-induced hyperalgesia paralleled estradiol changes during estropause: hyperalgesia first decreased, then returned. Furthermore, the return occurred regardless of the presence of the cysts (excised in some rats). This finding provides further support for ENDO's likely centrally-mediated effects. Additionally, the results suggest that elimination of estradiol via ovariectomy (OVX) should alleviate ENDO-induced hyperalgesia and estradiol replacement should restore it. However, in healthy and shamENDO rats, OVX produces a vaginal hyperalgesia that is alleviated by estradiol, likely via estradiol's peripheral influences on the vagina. Hence, we tested the hypothesis that OVX in ENDO rats would trigger a different type of vaginal hyperalgesia dependent on the loss of estradiol. We predicted that the opposing influences of estradiol on ENDO-and OVX-induced hyperalgesia would cancel each other. As predicted, OVX had no effect on ENDO-induced hyperalgesia and estradiol replacement alleviated it. These results suggest that, in intact rats, ENDO-induced vaginal hyperalgesia is exacerbated by estradiol, and that different mechanisms underlie ENDO-induced versus OVXinduced vaginal hyperalgesia.

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Section: Mechanisms Of Endo-induced Versus Ovx-induced Vaginal Hyperamentioning

confidence: 99%

Endometriosis-induced vaginal hyperalgesia in the rat: Effect of estropause, ovariectomy, and estradiol replacement

Berkley

McAllister

Accius

et al. 2007

Pain

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“…In contrast, the chronic pain conditions such as irritable bowel syndrome, interstitial cystitis, and orofacial pain are more prevalent in females than in males [15,16]. The threshold to evoke a visceromotor reflex or pressor response to colorectal distention or to activate uterine and vaginal primary afferents is lowest in proestrus [17][18][19]. Although the reason for this discrepancy is unclear, estrogen modulation of pain is highly specific to the type of nociceptive test, the occurrence of pain, and the characteristics of pain syndromes developed [3,20].…”

mentioning

confidence: 96%

Estrogen modulation of peripheral pain signal transduction: involvement of P2X3 receptors

Jin

et al. 2011

Purinergic Signalling

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There is evidence that gonadal hormones may affect the perception of painful stimulation, although the underlying mechanisms remain unclear. This investigation was undertaken to determine whether the adenosine 5′-triphosphate (ATP) receptor subunit, P2X 3 , is involved in the modulatory action of estrogen in peripheral pain signal transduction in dorsal root ganglion (DRG). The mechanical pain behavior test, real-time quantitative reverse transcription-polymerase chain reaction analysis, and Western blot methods were used to determine the mean relative concentrations and functions of P2X 3 receptors in DRG in sham, ovariectomized (OVX), and estradiol replacement (OVX+E 2 ) female rats and in sham and orchiectomized male rats. The mechanical hyperalgesia appeared after ovariectomy, which was subsequently reversed after estradiol replacement, whereas it was not observed after orchiectomy in male rats. Plantar injection of 2′(3′)-O-(2,4,6-trinitrophenyl) ATP (TNP-ATP), a P2X 3 and P2X 2/3 receptor antagonist, resulted in an increase of the pain threshold force in OVX rats while had no effect on sham rats. Furthermore, A-317491, a selective P2X 3 /P2X 2/3 receptor antagonist, significantly reversed the hyperalgesia of OVX rats. Injection of ATP into the plantars also caused a significant increase of the paw withdrawal duration in OVX rats compared with that seen in the sham group, which became substantially attenuated by TNP-ATP. P2X 3 receptors expressed in DRG were significantly increased in both mRNA and protein levels after ovariectomy and then reversed after estrogen replacement, while a similar increase was not observed after orchiectomy in male rats. Furthermore, P2X 3 mRNA was significantly decreased 24 h after the application of 17β-estradiol in a concentrationdependent manner in cultured DRG neurons. ICI 182,780, an estrogen receptor antagonist, blocked the reduction in the protein level. These results suggest that the female gonadal hormone, 17β-estradiol, might participate in the control of peripheral pain signal transduction by modulating P2X 3 receptor-mediated events in primary sensory neurons, probably through genomic mechanisms.

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“…Part of the reason for this conclusion is that the pattern of estrous changes in the afferent fibers differs from those found here in NG. For example, whereas the percentage of neurons in NG responding to vaginal distention did not vary with estrous stage and their response latency was longer in D than in P and E, the response threshold of fibers in the pelvic nerve to distention of the vaginal canal was lower in P than in the other three stages (Robbins et al, 1992). The main reason, however, is that the overall percentages of responses of NG neurons to visceral stimulation did not change with estrous stage.…”

Section: Responses To Visceral Stimulationmentioning

confidence: 46%

“…Although sensory neurons that innervate the pelvic viscera express estrogen receptors and show estrous variations in responses to distention of the vaginal canal and uterus (Robbins et al, 1992), it seems unlikely that these afferents are a major source of visceral response variations in NG. Part of the reason for this conclusion is that the pattern of estrous changes in the afferent fibers differs from those found here in NG.…”

Section: Responses To Visceral Stimulationmentioning

confidence: 99%

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

Bradshaw

Berkley

2000

J. Neurosci.

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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...

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Estrous cycle variation of afferent fibers supplying reproductive organs in the female rat

Cited by 91 publications

References 19 publications

Endometriosis-induced vaginal hyperalgesia in the rat: Effect of estropause, ovariectomy, and estradiol replacement

Endometriosis-induced vaginal hyperalgesia in the rat: Effect of estropause, ovariectomy, and estradiol replacement

Estrogen modulation of peripheral pain signal transduction: involvement of P2X3 receptors

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

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