Carol A. Dudley

University of Texas Southwestern Medical Center, Dallas, Texas, United States

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Publications (68)283.32 Total impact

  • Article: Pheromones
    A. Kumar · C.A. Dudley · S. Chakravarty · R.L. Moss
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    ABSTRACT: Pheromone detection is an important component in the animal's ability to respond appropriately to social cues, such as sexual and stressful signals, in social and agonistic interactions. Several mammalian species experiencing stress and fear release chemosignals that induce behavioral, endocrinological, and immunological changes in the recipient animals of the same species. Aggressive behavior is displayed in many species in day-to-day social interactions. This behavior is elicited by appropriate recognition of an adversary as a potential threat or sexual competitor, and this recognition involves the detection of social odors by the vomeronasal and/or olfactory systems. However, mechanisms underlying the vomeronasal-dependent responses to sociogenic stress are largely unknown at this time.
    No preview · Article · Jan 2010
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    ABSTRACT: Because the transcription factor neuronal Per-Arnt-Sim-type signal-sensor protein-domain protein 2 (NPAS2) acts both as a sensor and an effector of intracellular energy balance, and because sleep is thought to correct an energy imbalance incurred during waking, we examined NPAS2's role in sleep homeostasis using npas2 knockout (npas2-/-) mice. We found that, under conditions of increased sleep need, i.e., at the end of the active period or after sleep deprivation (SD), NPAS2 allows for sleep to occur at times when mice are normally awake. Lack of npas2 affected electroencephalogram activity of thalamocortical origin; during non-rapid eye movement sleep (NREMS), activity in the spindle range (10-15 Hz) was reduced, and within the delta range (1-4 Hz), activity shifted toward faster frequencies. In addition, the increase in the cortical expression of the NPAS2 target gene period2 (per2) after SD was attenuated in npas2-/- mice. This implies that NPAS2 importantly contributes to the previously documented wake-dependent increase in cortical per2 expression. The data also revealed numerous sex differences in sleep; in females, sleep need accumulated at a slower rate, and REMS loss was not recovered after SD. In contrast, the rebound in NREMS time after SD was compromised only in npas2-/- males. We conclude that NPAS2 plays a role in sleep homeostasis, most likely at the level of the thalamus and cortex, where NPAS2 is abundantly expressed.
    Full-text · Article · Jun 2006 · Proceedings of the National Academy of Sciences
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    ABSTRACT: The neuronal PAS domain protein 3 (NPAS3) gene encoding a brain-enriched transcription factor was recently found to be disrupted in a family suffering from schizophrenia. Mice harboring compound disruptions in the NPAS3 and related NPAS1 genes manifest behavioral and neuroanatomical abnormalities reminiscent of schizophrenia. Herein we demonstrate that Npas3-/- mice are deficient in expression of hippocampal FGF receptor subtype 1 mRNA, most notably in the dentate gyrus. In vivo BrdUrd-labeling shows that basal neural precursor cell proliferation in the dentate gyrus of Npas3-/- mice is reduced by 84% relative to wild-type littermates. We propose that a deficiency in adult neurogenesis may cause the behavioral and neuroanatomical abnormalities seen in Npas3-/- mice, and we speculate that impaired neurogenesis may be involved in the pathophysiology of schizophrenia.
    Full-text · Article · Oct 2005 · Proceedings of the National Academy of Sciences
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    ABSTRACT: Laboratory mice bearing inactivating mutations in the genes encoding the NPAS1 and NPAS3 transcription factors have been shown to exhibit a spectrum of behavioral and neurochemical abnormalities. Behavioral abnormalities included diminished startle response, as measured by prepulse inhibition, and impaired social recognition. NPAS1/NPAS3-deficient mice also exhibited stereotypic darting behavior at weaning and increased locomotor activity. Immunohistochemical staining assays showed that the NPAS1 and NPAS3 proteins are expressed in inhibitory interneurons and that the viability and anatomical distribution of these neurons are unaffected by the absence of either transcription factor. Adult brain tissues from NPAS3- and NPAS1/NPAS3-deficient mice exhibited a distinct reduction in reelin, a large, secreted protein whose expression has been reported to be attenuated in the postmortem brain tissue of patients with schizophrenia. These observations raise the possibility that a regulatory program controlled in inhibitory interneurons by the NPAS1 and NPAS3 transcription factors may be either substantively or tangentially relevant to psychosis.
    Full-text · Article · Oct 2004 · Proceedings of the National Academy of Sciences
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    ABSTRACT: Animal behavior is synchronized to the 24-hour light:dark (LD) cycle by regulatory programs that produce circadian fluctuations in gene expression throughout the body. In mammals, the transcription factor CLOCK controls circadian oscillation in the suprachiasmatic nucleus of the brain; its paralog, neuronal PAS domain protein 2 (NPAS2), performs a similar function in other forebrain sites. To investigate the role of NPAS2 in behavioral manifestations of circadian rhythm, we studied locomotor activity, sleep patterns, and adaptability to both light- and restricted food-driven entrainment in NPAS2-deficient mice. Our results indicate that NPAS2 plays a substantive role in maintaining circadian behaviors in normal LD and feeding conditions and that NPAS2 is critical for adaptability to food restriction.
    No preview · Article · Aug 2003 · Science
  • Carol A Dudley · Sumana Chakravarty · Ayalla Barnea
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    ABSTRACT: Pheromonal mediation of reproductive function proceeds along a neuroanatomical pathway that connects the vomeronasal organ (VNO) at the periphery with downstream target-sites in the amygdala and hypothalamus. The MAPK pathway is a prominent cascade linking receptor activation to induction of effectors such as c-Fos. We addressed the question: Does a specific pheromone stimulus lead to activation (phosphorylation, P) of MAPK in the VN system of the male mouse? Phosphorylation of MAPK in the VN system was evaluated 15-30 min and 1.5-2 h after exposure to female odors, using immunocytochemical techniques. A rapid and transient cytoplasmic expression of PMAPK was noted in the VNO with a unique distribution of the expressing neurons in columns extending over the entire basal to apical axis. A rapid and sustained expression was noted in most amygdaloid and hypothalamic VN target-sites and also in a few amygdaloid and hypothalamic sites outside the traditional VN system. The extent of expression and the subcellular compartmentalization (nucleus, cytoplasm, processes) of PMAPK were region-dependent. Of the VN target-sites, the accessory olfactory bulb (AOB) stood out in the lack of expression of PMAPK, in the high expression of the MAPK enzyme itself and in the massive of expression of c-Fos. This expression profile implicates another pathway(s) in mediating VNO signaling to the AOB. Our results are the first to demonstrate the use of PMAPK to trace functional pathways. Based on the wide cellular and intracellular expression of phosphorylated MAPK in the VN system, we propose that the MAPK pathway plays an important role in mediating female pheromone signaling in the male mouse.
    No preview · Article · Nov 2001 · Brain Research
  • M Reick · JA Garcia · C Dudley · S L McKnight
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    ABSTRACT: Neuronal PAS domain protein 2 (NPAS2) is a transcription factor expressed primarily in the mammalian forebrain. NPAS2 is highly related in primary amino acid sequence to Clock, a transcription factor expressed in the suprachiasmatic nucleus that heterodimerizes with BMAL1 and regulates circadian rhythm. To investigate the biological role of NPAS2, we prepared a neuroblastoma cell line capable of conditional induction of the NPAS2:BMAL1 heterodimer and identified putative target genes by representational difference analysis, DNA microarrays, and Northern blotting. Coinduction of NPAS2 and BMAL1 activated transcription of the endogenous Per1, Per2, and Cry1 genes, which encode negatively activating components of the circadian regulatory apparatus, and repressed transcription of the endogenous BMAL1 gene. Analysis of the frontal cortex of wild-type mice kept in a 24-hour light-dark cycle revealed that Per1, Per2, and Cry1 mRNA levels were elevated during darkness and reduced during light, whereas BMAL1 mRNA displayed the opposite pattern. In situ hybridization assays of mice kept in constant darkness revealed that Per2 mRNA abundance did not oscillate as a function of the circadian cycle in NPAS2-deficient mice. Thus, NPAS2 likely functions as part of a molecular clock operative in the mammalian forebrain.
    No preview · Article · Aug 2001 · Science
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    ABSTRACT: The vomeronasal organ is a chemoreceptive structure located at the base of the nasal septum with direct axonal connections to the accessory olfactory bulb in many terrestrial vertebrates. Pheromones presumably bind to the vomeronasal organ and exert behavioral or physiologic responses, thereby allowing chemical communication between animals of the same species. The presence and function of the vomeronasal organ in humans is debated. A phenotypic classification schema for the human vomeronasal organ is described and applied to 253 human subjects who underwent nasal examination. Of these subjects, only 6 percent possessed a vomeronasal organ with 64 percent unilateral and 36 percent bilateral in appearance. No difference existed in gender, age, or race between those subjects with or without a vomeronasal organ. There is no evidence supporting involutional senescence of this structure. Future investigations should use this phenotypic schema for the vomeronasal organ to allow accurate comparisons of study populations.
    No preview · Article · May 2000 · Plastic & Reconstructive Surgery
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    ABSTRACT: The aims of this study are to identify the sex steroid-metabolizing cytochrome P450 enzymes of the vomeronasal organ (VNO) and to determine the activities of VNO microsomes to metabolize estradiol, progesterone, and testosterone. Several P450 isoforms, including CYP1A2, CYP2A, CYP2B, CYP2C, CYP2G1, and CYP3A, NADPH P450-reductase, and microsomal epoxide hydrolase were detected in mouse VNO, although their expression levels were much lower than those in the main olfactory epithelium. VNO microsomes were active toward the three steroid hormones, producing metabolite profiles similar to those seen with olfactory mucosal microsomes. Thus, the mammalian VNO, a steroid hormone target tissue, contains multiple steroid-metabolizing P450 isoforms and is capable of metabolic disposition of the three major sex steroid hormones. These findings support the proposed roles of olfactory mucosal and VNO microsomal P450 enzymes in maintaining cellular hormonal homeostasis and other perireceptor processes associated with olfactory chemosensory function.
    No preview · Article · Jan 2000 · Biochemical and Biophysical Research Communications
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    A Kumar · CA Dudley · R L Moss
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    ABSTRACT: Chemosensory neurons in the vomeronasal organ (VNO) detect pheromones that elicit social and reproductive behaviors in most terrestrial vertebrates. Vomeronasal receptor neurons are chemoarchitecturally divided into two populations based on their position in the VNO, the type of G-protein subunit expressed, the family of putative pheromone receptor expressed, and termination site of their axons in the accessory olfactory bulb (AOB). To investigate the functional implications of these two segregated VNO-AOB pathways, we stimulated mice with pheromonal cues associated with different behavioral contexts and examined cellular activation patterns in the AOB. Exposure of ICR male mice to BALB/c males resulted in aggressive behavior, accompanied by a VNO-dependent increase in c-fos immunoreactivity in a cluster of cells located almost exclusively in the caudal AOB in both strains. This caudal cluster of activated cells did not appear to require the overt display of aggressive behavior because it was present in both the dominant and submissive males and could be evoked when the stimulus animal was anesthetized. In contrast, exposure of an ICR male to an ICR female in diestrus resulted in activation of cells located predominantly in the rostral AOB. Our findings indicate that male-to-male interactions involving interstrain recognition activate a separate population of vomeronasal receptor neurons than chemosensory cues detected in a sexual context. The results suggest that the dichotomy in the peripheral vomeronasal system serves to separate pheromones based on the behaviors they drive. As such, the results provide a bioassay for identifying pheromone molecules.
    Preview · Article · Nov 1999 · The Journal of Neuroscience : The Official Journal of the Society for Neuroscience
  • C.A Dudley · R L Moss
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    ABSTRACT: Chemosensory cues known as pheromones play a key role in rodent reproductive physiology and social interactions. Pheromone molecules are detected by receptor cells located in the vomeronasal organ and conveyed exclusively to the accessory olfactory bulb, and then to limbic and hypothalamic sites for integration with other factors modulating reproductive physiology. We report here that chemosensory cues from the female mouse selectively activate a subpopulation of cells located in the anterior part of the accessory olfactory bulb of the male mouse. Exposure of male mice to female-soiled bedding resulted in a massive induction of c-fos expression, which was primarily confined to neurons located in the anterior part of the accessory olfactory bulb and was eliminated by removal of the vomeronasal organ. Exposure of the male to soiled bedding from a different stain of male mice also elevated c-fos expression, but immunoreactive cells were more evenly distributed along the anterior-posterior axis of the accessory olfactory bulb. No treatment effects were observed in the main olfactory bulb. Previous studies have indicated that vomeronasal receptor neurons are divided into two populations based on location within the organ, site of termination in the accessory olfactory bulb, second messenger content and putative pheromone receptor expression. The present study suggests that the two populations of vomeronasal receptor neurons detect different chemosensory stimuli. Since male mouse- and female mouse-specific urinary substances modulate different aspects of male mouse behavior, the present results suggest that anatomically segregated populations of vomeronasal organ receptor cells modulate distinct behavioral patterns.
    No preview · Article · Feb 1999 · Neuroscience
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    R L Moss · R E Flynn · JM Shi · X M Shen · C Dudley · A Zhou · M Novotny
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    ABSTRACT: Receptor cells of the vomeronasal organ (VNO) are thought to detect pheromone-like molecules important for reproductive physiology. Several compounds derived from male mouse urine have been demonstrated to affect endocrine events in female mice. In the present study, the ability of these compounds to affect VNO activity was tested. In dissociated VNO cells held under voltage clamp conditions, application of dehydro-exo-brevicomin (DHB) evoked an outward current at negative holding potentials and an inward current at positive holding potentials. Under current clamp, DHB reduced action potential firing. Since DHB application caused a decrease in membrane conductance, this compound appeared to act by reducing inward current through closing an ion channel. Biochemical experiments tested the effects of DHB and 2-(sec-butyl)-4,5-dihydrothiazole (SBT) on cAMP levels in the VNO. A mixture of DHB and SBT decreased cAMP levels in VNO sensory tissue and had no effect on VNO non-sensory tissue. The results suggest that pheromones have an inhibitory influence on action potential generation and on cAMP levels in receptor cells of the VNO.
    Full-text · Article · Sep 1998 · Chemical Senses
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    Preview · Article · Aug 1998 · Chemical Senses
  • R L Moss · R E Flynn · X M Shen · C Dudley · Shi JM · M Novotny
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    ABSTRACT: Sensory neurons of the vomeronasal organ (VNO) are thought to detect species-specific chemical signals important for reproductive function. The electrical properties of VNO neurons have begun to be characterized in a variety of species; however, the response of VNO neurons to possible physiological ligands has not yet been reported. One physiological effector, dehydro-exo-brevicomin (DHB), is found in the urine of intact male mice and affects the estrous cycle of female mice. In the present study, dissociated VNO neurons were voltage- or current-clamped and their response to DHB was determined. Approximately 26% of VNO neurons responded to DHB with an outward current at negative holding potentials; the current reversed at approximately +4 mV. Application of DHB in current-clamp mode produced membrane hyperpolarization and/or a reduction in the firing of action potentials. Because membrane conductance was shown to be decreased during application of DHB, the results suggest that the outward current associated with DHB application is a reflection of a reduction in inward current caused by closing an ion channel. This study provides the first evidence that a compound found in male urine directly affects VNO neurons.
    No preview · Article · Jun 1997 · Journal of Neurophysiology
  • Carol A. Dudley · Gopalan Rajendren · Robert L. Moss
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    ABSTRACT: Chemosensory cues detected by the vomeronasal (VN) organ modulate a variety of social interactions in many species. In particular, activation of the VN system by pheromones regulates sexual behavior in the rodent. Although the exact nature of stimulus access to the organ is not clearly defined, the neuroanatomical pathway connecting the VN organ to hypothalamic centers controlling reproductive function is well established and relatively straightforward. Electrophysiological techniques have provided insight into the signal transduction process throughout the VN system. Combining behavioral studies with immunocytochemical detection of immediate early genes and neuropeptides reveals that gonadotropin hormone releasing hormone (GnRH)-containing neurons are specifically activated by stimulation of the VN organ. Furthermore, some of the activated GnRH neurons project to the ventromedial hypothalamus where they are hypothesized to induce sexual responsiveness. Early anecdotal evidence of an influence of the VN organ on human reproductive events has been substantiated by more recent anatomical, behavioral, and electrophysiological studies. Thus, further deciphering of the signal transduction process within the VN system of the rodent may yield unique insights into behaviors associated with human reproduction.
    No preview · Article · Feb 1996 · Critical Reviews in Neurobiology
  • Carol A. Dudley · Robert L. Moss
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    ABSTRACT: Bipolar receptor cells in the vomeronasal organ send axonal projections to the accessory olfactory bulb where they synapse with mitral cell dendrites. Although the nature of the synapse is thought to be excitatory, the neurotransmitter(s) involved has not yet been identified. Electrophysiological recordings of single neurons in the mitral cell layer of the AOB in response to vomeronasal nerve stimulation were conducted to characterize the synaptic response and the underlying neurotransmitter substance. Extracellular activity was recorded in vivo (whole animal) and in vitro (AOB slice) from female rats. In vivo, the predominant response to stimulation of the VNO was excitation. In many instances in the whole animal preparation, the excitation was followed by an inhibitory response. Attempts to block the excitatory response by ejecting kynurenic acid in close proximity to the mitral cell being recorded were not successful. Since this failure may have been due to inability of the antagonist to reach its presumed site of action at the dendrite, further recordings were carried out in vitro. In the AOB slice preparation, the predominant response to stimulation of the VN nerve endings was excitation. Superfusion of the non-NMDA antagonist, CNQX, into the medium resulted in a reduction of the orthodromic excitation in 5 of 8 cells. The NMDA antagonist, AP-5, was found to blunt orthodromic excitation in 1 of 4 cells. These results suggest that the excitatory response evoked in mitral cells followng stimulation of the VN nerve is mediated by glutamate.
    No preview · Article · Apr 1995 · Brain Research
  • Carol A. Dudley · Robert L. Moss
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    ABSTRACT: The effect of bilateral lesion of the accessory olfactory bulb (AOB) on the mating-induced enhancement of sexual receptivity was investigated in ovariectomized (OVX) female rats. Lesions of the AOB significantly reduced the lordosis-to-mount (L/M) ratio in mating tests conducted 20 to 50 days after the lesion but L/M ratios at earlier (10 days) and later (51-90 days) time periods were not affected. The decrease in L/M was accompanied by a reduction in the number of c-fos immunopositive cells in the medial amygdala (mAMYG) and bed nucleus of the stria terminalis (BNST) measured after 3 h of repetitive mating. In the mAMYG, the reduction in c-fos immunoreactivity was correlated to the L/M ratio as well as to the number of intromissions received during the mating tests. The results suggest that information processed from the AOB to the mAMYG and the BNST is important for facilitation of lordosis behavior, and that the mAMYG may integrate information from the AOB with ascending input activated during copulatory behavior to regulate receptivity.
    No preview · Article · May 1994 · Brain Research
  • Gopalan Rajendren · Carol A. Dudley · Robert L. Moss
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    ABSTRACT: Olfactory information processed by the vomeronasal system is reported to influence reproductive functions in a variety of mammals. The present studies were designed to determine if male-associated cues affect the luteinizing hormone-releasing hormone (LHRH) neuronal system, and, if so, to determine the extent to which these cues are processed by the vomeronasal organ (VNO). Ovariectomized rats underwent VNO removal (VNX) or sham surgery (VN-Sham). Forty-eight hours after estrogen priming (5 micrograms), they were subjected to one of the following treatments: repeated mating, repeated exposure to male-soiled bedding or repeated exposure to clean bedding. In animals treated for 180 min, coronal brain sections were double labelled for Fos protein and LHRH. An intense Fos immunoreactivity was induced following mating in the majority of LHRH neurons in the VN-Sham females, whereas removal of the VNO significantly suppressed the mating-induced Fos staining. Exposure of female rats to male-soiled bedding or clean bedding did not induce appreciable Fos immunoreactivity in LHRH neurons. Following 90 min of mating or exposure to bedding, blood samples were assayed for luteinizing hormone (LH). Mating stimulated the release of LH in VN-Sham females, while the removal of the VNO significantly suppressed the mating-induced LH release. Exposure of the females to male-soiled bedding or clean bedding did not induce an LH surge. The present results demonstrate that male-originating sensory cues (i.e. repeated mating) can influence the LHRH neuronal system, as evidenced by the presence of Fos immunoreactivity in LHRH cell bodies, and indicate that this effect is mediated through the VNO to a certain extent.(ABSTRACT TRUNCATED AT 250 WORDS)
    No preview · Article · Jun 1993 · Neuroendocrinology
  • Carol A. Dudley · Skylar B. Sudderth · Robert L. Moss
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    ABSTRACT: While neurons containing immunoreactive luteinizing hormone-releasing hormone (LHRH) are scattered primarily in the medial septal-diagonal band of Broca-medial preoptic area (mS-dbB-PO) complex, autoradiographic studies have demonstrated dense concentrations of LHRH receptors in the hippocampus. The route by which LHRH is transported to its hippocampal receptors is unknown. The present study was designed to test the hypothesis that LHRH-containing neurons in the mS-dbB-PO complex project to hippocampal sites containing LHRH receptors, thereby serving as a source of innervation to these receptors. Large (0.10 m̈l) or small (0.02 m̈l) volumes of the retrograde tracer wheat germ agglutinin (WGA) were injected unilaterally into four separate hippocampal locations in six ovariectomized female rats. In an additional five females, a 0.15 m̈l volume of the retrograde tracer fluorogold (FG) was similarly injected. After a five day survival period, the animals were sacrificed. Vibratome sections of the brain were stained for both WGA and LHRH with a dual immunohistochemical technique. Since FG is a fluorescent chromagen, brains of animals injected with FG only required processing for LHRH immunofluorescence. As a positive control, some sections containing retrogradely labeled cells filled with either WGA or FG were processed for choline acetyltransferase (CHAT) immunoreactivity. The WGA and FG injections covered targeted hippocampal sites and neurons containing retrogradely transported WGA or FG were found in abundance in the mS-dbB-PO complex. In accord with previous reports, many CHAT-positive and fewer LHRH-positive neurons were found in this complex. Approximately 5–10% of the CHAT-positive neurons also contained WGA or FG; however, no neurons were found to co-localize LHRH and either of the retrograde tracers. The results indicate that LHRH neurons in the mS-dbB-PO complex do not project directly to hippocampal sites containing LHRH receptors.
    No preview · Article · Oct 1992 · Synapse
  • CA Dudley · G Rajendren · R L Moss
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    ABSTRACT: Reproductive events in the female rat can be influenced by exposure to the odors of conspecific males. Much evidence indicates that these pheromonal effects are mediated by the accessory olfactory system (AOS); however, individual cells within the AOS that are stimulated following exposure to male odors have not yet been visualized. The present experiment was designed to determine the effect of exposure to conspecific males and male odors on signal transduction in central AOS neurons as measured by immunohistochemical detection of the induction of the fos-like protein. AOS structures examined included the accessory olfactory bulb (AOB), medial amygdala (mAMYG), and bed nucleus of the stria terminalis (BNST). Due to its importance in the control of reproductive activities and its direct link to the AOS, the ventromedial nucleus of the hypothalamus (VMH) was also examined. Adult, ovariectomized rats were injected with estradiol benzoate (EB) and 48 h later were placed in cages containing bedding material soiled by conspecific males or placed in cages containing clean bedding material. After exposure durations ranging from 10 to 180 min, the animals were sacrificed and the brains were immunohistochemically processed for detection of fos-like immunoreactivity. Another group of ovariectomized, EB-injected females was repeatedly paired with conspeciflc males for 15 min followed by 15 min of rest. Repeated matings were conducted over a 60-, 120-, or 180-min period while control animals were repeatedly exposed to clean bedding material. Quantitative analysis of the number of fos-immunopositive cells in the AOB revealed that continuous exposure to male-soiled bedding or repeated mating resulted in significant induction of foslike immunoreactivity compared to controls. Both treatments produced similar numbers of fos-like immunoreactive cells in the mitral and granule cell layers of the AOB. Fos induction was apparent after 60 min of treatment but was more prominent at 120 and 180 min. In the mAMYG, BLAST, and VMH, differences between the two treatments were noted. Exposure to male-soiled bedding for 60 min produced scattered staining in the mAMYG, BLAST, and VMH, whereas 60 min of repetitive mating resulted in a more dense distribution of fos-like immunoreactive cells in these areas. Strikingly distinct patterns of fos-like immunoreactive cells were observed in the mAMYG, BLAST, and VMH following 120 or 180 min of repetitive mating. These patterns were not present in animals exposed to male odors. The findings indicate that exposure of female rats to reproductively relevant stimuli resulted in induction of fos-like immunoreactivity within the AOS and that both olfactory and nonolfactory cues probably contributed to this effect.
    No preview · Article · Aug 1992 · Molecular and Cellular Neuroscience

Publication Stats

3k Citations
283.32 Total Impact Points


  • 1988-2006
    • University of Texas Southwestern Medical Center
      • • Department of Biochemistry
      • • Department of Physiology
      Dallas, Texas, United States
  • 1991
    • University of Texas at Dallas
      Richardson, Texas, United States
  • 1977-1988
    • University of Texas Health Science Center at Tyler
      Tyler, Texas, United States
  • 1984
    • University of North Texas at Dallas
      Dallas, Texas, United States
  • 1983
    • Salk Institute
      لا هویا, California, United States