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1.
Neuroscience ; 237: 170-83, 2013 May 01.
Article in English | MEDLINE | ID: mdl-23395860

ABSTRACT

The inferior colliculus (IC) integrates ascending auditory input from the lower brainstem and descending input from the auditory cortex. Understanding how IC cells integrate these inputs requires identification of their synaptic arrangements. We describe excitatory synapses in the dorsal cortex, central nucleus, and lateral cortex of the IC (ICd, ICc and IClc) in guinea pigs. We used electron microscopy (EM) and post-embedding anti-GABA immunogold histochemistry on aldehyde-fixed tissue from pigmented adult guinea pigs. Excitatory synapses were identified by round vesicles, asymmetric synaptic junctions, and gamma-aminobutyric acid-immunonegative (GABA-negative) presynaptic boutons. Excitatory synapses constitute ∼60% of the synapses in each IC subdivision. Three types can be distinguished by presynaptic profile area and number of mitochondrial profiles. Large excitatory (LE) boutons are more than 2 µm(2) in area and usually contain five or more mitochondrial profiles. Small excitatory (SE) boutons are usually less than 0.7 µm(2) in area and usually contain 0 or 1 mitochondria. Medium excitatory (ME) boutons are intermediate in size and usually contain 2 to 4 mitochondria. LE boutons are mostly confined to the ICc, while the other two types are present throughout the IC. Dendritic spines are the most common target of excitatory boutons in the IC dorsal cortex, whereas dendritic shafts are the most common target in other IC subdivisions. Finally, each bouton type terminates on both gamma-aminobutyric acid-immunopositive (GABA+) and GABA-negative (i.e., glutamatergic) targets, with terminations on GABA-negative profiles being much more frequent. The ultrastructural differences between the three types of boutons presumably reflect different origins and may indicate differences in postsynaptic effect. Despite such differences in origins, each of the bouton types contact both GABAergic and non-GABAergic IC cells, and could be expected to activate both excitatory and inhibitory IC circuits.


Subject(s)
Inferior Colliculi , Microscopy, Immunoelectron , Neurons/ultrastructure , Synapses/physiology , Synapses/ultrastructure , gamma-Aminobutyric Acid/metabolism , Animals , Female , Guinea Pigs , Inferior Colliculi/cytology , Inferior Colliculi/metabolism , Inferior Colliculi/ultrastructure , Male , NADPH Dehydrogenase/metabolism , Neurons/metabolism , Presynaptic Terminals/metabolism , Presynaptic Terminals/ultrastructure
2.
Peptides ; 27(4): 743-52, 2006 Apr.
Article in English | MEDLINE | ID: mdl-16181705

ABSTRACT

The uterine cervix is highly innervated by the sensory nerves containing neuropeptides which change during pregnancy and are regulated, in part, by estrogen. These neuropeptides act as transmitters both in the spinal cord and cervix. The present study was undertaken to determine the expression pattern of the neuropeptide pituitary adenylate cyclase activating peptide (PACAP) in the cervix and its nerves during pregnancy and the influence of estrogen on this expression using immunohistochemistry, radioimmunoassay and RT-PCR. PACAP immunoreactivity was detected in nerves in the cervix, lumbosacral (L6-S1) dorsal root ganglia (DRG) and spinal cord. PACAP immunoreactivity was highest at day 15 of pregnancy in the cervix and dorsal spinal cord, but then decreased over the last trimester of pregnancy. However, levels of PACAP mRNA increased in the L6-S1 DRG at late pregnancy relative to early pregnancy. DRG of ovariectomized rats treated with estrogen showed increased PACAP mRNA synthesis in a dose-related manner, an effect partially blocked by the estrogen receptor (ER) antagonist ICI 182,780. We postulate that synthesis of PACAP in L6-S1 DRG and utilization in the cervix and spinal cord increase over pregnancy and this synthesis is the under influence of the estrogen-ER system. Since PACAP is expressed by sensory nerves and may have roles in nociception and vascular function, collectively, these data are consistent with the hypothesis that sensory nerve-derived neuronal factors innervate the cervix and play a role in cervical ripening.


Subject(s)
Cervix Uteri/metabolism , Ganglia, Spinal/metabolism , Gene Expression Regulation , Pituitary Adenylate Cyclase-Activating Polypeptide/genetics , Pituitary Adenylate Cyclase-Activating Polypeptide/metabolism , Spinal Cord/metabolism , Animals , Female , Pregnancy , RNA, Messenger , Rats , Time Factors
3.
Peptides ; 24(8): 1163-74, 2003 Aug.
Article in English | MEDLINE | ID: mdl-14612187

ABSTRACT

Before parturition the uterine cervix undergoes a ripening process ("softens" and dilates) to allow passage of the fetus at term. The exact mechanism(s) responsible for cervical ripening are unknown, though a role for peptidergic sensory neurons is emerging. Previous work demonstrated that administration of substance P (SP) to ovariectomized rats caused events associated with cervical ripening, that production of SP in cervix-related dorsal root ganglion (DRG) is estrogen responsive, and that release of SP from neurons terminating in the cervix and spinal cord peaks prior to parturition. The present study was designed to test the hypothesis that calcitonin gene-related peptide (CGRP), a neuropeptide co-stored with SP in many sensory neurons, undergoes changes with pregnancy and hormonal environment. Immunohistochemistry, in situ hybridization, reverse transcriptase-polymerase chain reaction (RT-PCR) and radioimmunoassay (RIA) were used to investigate CGRP in L6-S1 DRG, spinal cord and cervix during pregnancy and the role of estrogen in CGRP synthesis. CGRP-immunoreactive primary sensory neurons expressed estrogen receptors (ER-alpha and ER-beta). In the cervix, CGRP concentrations decreased, but in the L6-S1 DRG and the spinal cord segments, CGRP levels increased, with peak effects observed at day 20 of gestation. CGRP mRNA synthesis increased in DRG over pregnancy. Sensory neurons of ovariectomized rats treated with estrogen showed increased CGRP mRNA synthesis in a dose-related manner, an effect blocked by the ER antagonist ICI 182 780. From these results, we postulate that synthesis of CGRP in L6-S1 DRG and utilization in the cervix increase over pregnancy and this synthesis is the under influence of the estrogen-ER system. Collectively, these data are consistent with the hypothesis that CGRP plays a role in cervical ripening and, consequently in the birth process.


Subject(s)
Calcitonin Gene-Related Peptide/genetics , Cervix Uteri/physiology , Estrogens/physiology , Ganglia, Spinal/physiology , Spinal Cord/physiology , Animals , Calcitonin Gene-Related Peptide/analysis , Calcitonin Gene-Related Peptide/biosynthesis , Female , Immunohistochemistry , In Situ Hybridization , Pregnancy , RNA, Messenger/metabolism , Radioimmunoassay , Rats , Rats, Sprague-Dawley
4.
Peptides ; 24(5): 761-71, 2003 May.
Article in English | MEDLINE | ID: mdl-12895664

ABSTRACT

Prior to parturition the non-pliable uterine cervix undergoes a ripening process ("softens" and dilates) to allow a timely passage of the fetus at term. The exact mechanism(s) triggering and involved in cervical ripening are unknown, though evidence for a role for sensory neurons and their contained neuropeptides is emerging. Moreover, an apparent increase in neuropeptide immunoreactive nerves occurs in the cervix during pregnancy, maternal serum estrogen levels rise at term and uterine cervix-related L6-S1 dorsal root ganglia (DRG) sensory neurons express estrogen receptor (ER) and neuropeptides. Thus, we sought to test the hypothesis that the neuropeptide substance P (SP) changes biosynthesis and release over pregnancy, that estrogen, acting via the ER pathway, increases synthesis of SP in DRG, and that SP is utilized in cervical ripening at late pregnancy. Using immunohistochemistry, in situ hybridization, reverse transcriptase-polymerase chain reaction (RT-PCR) and radioimmunoassay (RIA), we investigated coexpression of ER-alpha/beta and SP; differential expression of ER-alpha and -beta mRNA in DRG neurons; SP synthesis in DRG; and changes in SP concentration in the cervix, DRG and spinal cord over pregnancy. In addition, the effect of exogenous estrogen on SP synthesis in L6-S1 DRG of ovariectomized rats was examined. SP-immunoreactive neurons expressed ER-alpha and ER-beta. SP synthesis (expressed as beta-PPT mRNA label) was prominent in small DRG neurons. SP concentration increased in the L6-S1 DRG and spinal cord segments, with a peak at Day 20 of gestation, but decreased in the cervix during the first two trimesters, with a rise over the last trimester to Day 10 levels. SP and ER-alpha mRNA synthesis increased in DRG over pregnancy but ER-beta mRNA levels were largely unchanged. When ovariectomized rats were treated with exogenous estrogen, SP mRNA synthesis in the DRG increased in a dose-related manner, an effect blocked by ER blocker ICI 182 780. From these results, we postulate that synthesis of SP in L6-S1 DRG and utilization in the cervix increase over pregnancy and this synthesis is under influence of the estrogen-ER system, most likely ER-alpha. We postulate that SP may play a role in cervical ripening and, consequently in the birth process.


Subject(s)
Cervix Uteri/metabolism , Estradiol/analogs & derivatives , Estrogens/pharmacology , Ganglia, Spinal/metabolism , Pregnancy/metabolism , Spinal Cord/metabolism , Substance P/biosynthesis , Animals , Cervix Uteri/cytology , Down-Regulation , Estradiol/pharmacology , Female , Fulvestrant , Ganglia, Spinal/cytology , Immunohistochemistry , In Situ Hybridization , Neurons, Afferent/metabolism , Postpartum Period , RNA, Messenger/genetics , RNA, Messenger/metabolism , Radioimmunoassay , Rats , Rats, Sprague-Dawley , Receptors, Estrogen/antagonists & inhibitors , Reverse Transcriptase Polymerase Chain Reaction , Spinal Cord/cytology , Substance P/genetics , Substance P/metabolism , Up-Regulation
5.
J Neurosci Res ; 70(6): 808-16, 2002 Dec 15.
Article in English | MEDLINE | ID: mdl-12444603

ABSTRACT

Estrogen receptor immunoreactivity and mRNAs are present in spinal cord neurons in locations that are associated with sensory and autonomic innervation of female reproductive organs. The present study was undertaken to examine the expression of estrogen receptor-alpha in the spinal cord during different stages of pregnancy and to determine whether estrogen receptor-alpha-expressing neurons are related to uterine afferent nerves bringing information to the spinal cord at parturition. Immunohistochemistry showed estrogen receptor-alpha-immunoreactive neurons in the dorsal one-half of the spinal cord, i.e., dorsal horn, dorsal intermediate gray areas (dorsal commissural nucleus), and around the central canal and sacral parasympathetic autonomic nucleus of the lumbosacral spinal cord. Neurons in these areas corresponded topographically to the distribution of central processes of visceral primary afferent neurons (e.g., containing calcitonin gene-related peptide and substance P) that innervate and activate second-order spinal cord neurons (evidenced by their expression of Fos) at parturition. Western blots showed that estrogen receptor-alpha increases in the spinal cord, with a peak at day 20 of gestation, followed by a slight decrease by 2 days postpartum. These studies show that estrogen receptor-alpha is expressed by neurons in autonomic and sensory areas of the lumbosacral spinal cord that have connections with the female reproductive system and that the level of estrogen receptor-alpha changes over the course of pregnancy, which may follow profiles of steroid hormones. Many of these neurons may be involved in processing information related to reproductive organ function, changes during pregnancy, and relays to other CNS centers.


Subject(s)
Estrogens/physiology , Neurons, Afferent/metabolism , Pregnancy, Animal/physiology , Proto-Oncogene Proteins c-fos/biosynthesis , Receptors, Estrogen/biosynthesis , Animals , Blotting, Western , Estrogen Receptor alpha , Female , Ganglia, Autonomic/anatomy & histology , Ganglia, Autonomic/metabolism , Ganglia, Sensory/anatomy & histology , Ganglia, Sensory/metabolism , Immunohistochemistry , Parturition/physiology , Pregnancy , Rats , Rats, Sprague-Dawley , Spinal Cord/anatomy & histology , Spinal Cord/metabolism , Time Factors , Uterus/innervation
6.
Cell Tissue Res ; 304(2): 193-214, 2001 May.
Article in English | MEDLINE | ID: mdl-11396714

ABSTRACT

Estrogen receptor-alpha immunoreactivity and mRNAs are present in neurons in locales that innervate genital organs, e.g., parasympathetic pelvic autonomic ganglia, sensory dorsal root and nodose ganglia, and autonomic areas of the lumbosacral spinal cord. With the availability of probes for the beta-isoform of the estrogen receptor, we studied this receptor in autonomic, sensory, and spinal cord neurons and compared it with the distribution of the alpha-receptor. Estrogen receptor-alpha and -beta immunoreactivity were located in the nuclei of neurons, were in subpopulations of parasympathetic neurons in pelvic ganglia, and sensory neurons of dorsal root and nodose ganglia. Both receptor subtypes were present in the lumbosacral spinal cord: in neurons of the outer laminae of the dorsal horn, lateral collateral and medial collateral pathways, sacral parasympathetic nucleus, dorsal intermediate gray, and lamina X. Similar numbers of spinal cord neurons were immunoreactive for estrogen receptor-beta and estrogen receptor-alpha. However, estrogen receptor-beta-immunoreactive neurons appeared less numerous in the outer dorsal horn, but more numerous in the deeper layers of the spinal cord than estrogen receptor-alpha neurons. Retrograde tracing from the uterus revealed "uterine-related" neurons in dorsal root and pelvic ganglia that contained estrogen receptor-alpha and -beta. In situ hybridization revealed both estrogen receptor-alpha and -beta mRNA transcripts in sensory neurons of the dorsal root and nodose ganglia, parasympathetic neurons of pelvic ganglia, and spinal cord neurons in the dorsal horn, sacral parasympathetic nucleus, and dorsal intermediate gray of L6-S1 segments. These studies show that both estrogen receptor-alpha and -beta are synthesized by autonomic and sensory neurons in parts of the nervous system that have connections with the female reproductive system. Such neurons contain neurotransmitters that have important functions in the female reproductive organs; thus, it is likely that estrogen can influence the activity of such neurons and consequently, through them, the activities of the reproductive organs.


Subject(s)
Ganglia, Autonomic/metabolism , Ganglia, Sensory/metabolism , Neurons/metabolism , RNA, Messenger/metabolism , Receptors, Estrogen/analysis , Spinal Cord/metabolism , Animals , Calcitonin Gene-Related Peptide/metabolism , Estrogen Receptor alpha , Estrogen Receptor beta , Female , Ganglia, Autonomic/cytology , Ganglia, Sensory/cytology , Ganglia, Spinal/cytology , Ganglia, Spinal/metabolism , Immunohistochemistry , In Situ Hybridization , Neurons/cytology , Nodose Ganglion/cytology , Nodose Ganglion/metabolism , Ovariectomy , Rats , Rats, Sprague-Dawley , Receptors, Drug/metabolism , Receptors, Estrogen/immunology , Spinal Cord/cytology , Tissue Distribution , Uterus/innervation
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