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C-Fos Expression in Vomeronasal Pathways of Mated Or The Journal of Neuroscience, June 1994, 74(6): 3643-3654 c-fos Expression in Vomeronasal Pathways of Mated or Pheromone-stimulated Male Golden Hamsters: Contributions from Vomeronasal Sensory Input and Expression Related to Mating Performance Gwendolyn D. Fernandez-Fewell and Michael Meredith Program in Neuroscience, Department of Biological Science, Florida State University, Tallahassee, Florida 32306 The vomeronasal system projects to the accessory olfactory [Key words: vomeronasal, Fos, sex behavior, hamster, ac- bulb (AOB), to the medial (Me) and posterior medial cortical cessory olfactory, chemosensory, amygdala, bed nucleus nuclei (PMCN) of the amygdala, to the bed nucleus of the stria terminalis, medial preoptic] stria terminalis (BNST), and to other central structures shown to be important in mating behavior, including the medial The vomeronasal (VN) or accessoryolfactory system is a second preoptic area (MPOA). In these experiments c-fos expres- chemosensory system organized in parallel with the main ol- sion was used as a marker of neural activity to identify the factory system, and with anatomically distinct pathways (Scalia contribution of vomeronasal sensory input during mating be- and Winans, 1975; Davis et al., 1978). The vomeronasal organs havior in male golden hamsters, either intact or with vome- (VNOs) are tubular structures lying bilaterally in the ventral ronasal organs removed (VNX). Inexperienced hamsters were part of the nasal cavity. Vomeronasal receptor neurons project either stimulated with a receptive female and allowed to to the accessoryolfactory bulb (AOB) (Barber and Raisman, mate, exposed to female hamster vaginal fluid (HVF), which 1974) from which fibers project to two parts of the amygdala, contains stimuli known to act through the VN system, or the medial nucleus (Me) and the posterior medial cortical nu- placed in a clean cage alone. Densely stained Fos-positive cleus (PMCN), collectively called the vomeronasal amygdala nuclei were evident in mated animals in the central VN path- (Kevetter and Winans, 1981 a). The vomeronasalamygdala, and way [AOB, Me, posterior medial BNST (pmBNST)] and a VN the AOB in somespecies, projects via the stria terminalis to the target area (MPOA). HVF-exposed animals showed Fos ex- medial bed nucleus of the stria terminalis (mBNST) (Scalia and pression in the AOB, Me, and BNST but not MPOA. Unstim- Winans, 1976; Davis and Macrides, 1978; Lehman and Winans, ulated animals showed almost no activation. Most VNX an- 1983). The Me also has projections via the ventral amygdaloid imals exposed to females did not mate, but performed intense pathway and the stria terminalis to the medial preoptic anterior chemoinvestigation. They had few Fos-positive nuclei in any hypothalamic area and BNST (Lehman and Winans, 1983) and of these areas except the caudal pmBNST. A few VNX an- these regions also project to the ventromedial nucleus of the imals that did mate had patterns of Fos activation that were hypothalamus (VmH). Thus, the accessoryolfactory systemhas similar but less intense than those of intact mating animals, relatively direct and restricted projections to central structures suggesting a selective activation of VN central pathways known to be involved in reproductive physiology and behavior. during mating regardless of VN sensory input. The main ol- In contrast, the second-orderprojections of the main olfactory factory system showed low levels of Fos expression in all system spread widely and make somewhat lessdirect connec- animals (stimulated and unstimulated). Fos expression in tions to structures related to reproduction. The main olfactory the MPOA and rostra1 pmBNST was seen only in mated an- bulb projects to the anterior olfactory nucleus and olfactory imals, suggesting that these regions are concerned with mat- tubercle as well as to pyriform, entorhinal, and lateral amyg- ing performance or its consequences, rather than the daloid regions (Scalia and Winans, 1976; Davis et al., 1978). chemosensory input that triggers it. Fos expression in the Nevertheless, there are projections from the lateral (olfactory) caudal encapsulated pmBNST was evident in all groups of amygdalato the vomeronasalamygdala (Krettek and Price, 1978; animals that performed chemosensory investigation, re- Kevetter and Winans, 1981b). Neurons in the vomeronasal gardless of VN status or mating, suggesting that this region amygdala can be driven by separatestimulation of both olfac- either directs or responds to chemosensory investigation. tory and vomeronasal systems,suggesting a possiblefunctional convergence in this region (Licht and Meredith, 1987). The importance of the VN systemhas been demonstratedby a num- Received July 29, 1993; revised Oct. 20, 1993; accepted Nov. 24, 1993. ber of lesion and behavioral studiesimplicating this system in We thank Alice G. Howard for assistance with histology, Dr. C. Ouimet for use of the vibratome, Charles Badland for photographic assistance, and Richard Bnmck several aspectsof chemical communication and reproductive for assistance with illustrations. We also thank an anonymous reviewer for helpful behavior in several species.In rodents, chemical signalsacting suggestions. This work was supported by NIH Grant DC 00906. through the VNO affect male sexual behavior (Powersand Win- Correspondence should be addressed to Dr. Michael Meredith, Department of Biological Science, Florida State University, Tallahassee, FL 32306-4075. ans, 197.5;Wysocki et al., 1982; Meredith, 1986) and hormonal Copyright 0 1994 Society for Neuroscience 0270-6474/94/143643-12$05.00/O responsesto the opposite sex (Wysocki et al., 1983; Coquelin 3644 Fernandez-Fewell and Meredith * c-fos, VNO Pathways, and Behavior et al., 1984), as well as some aspects of female sexual behavior Materials and Methods (Saito and Moltz, 1986), estrus cycling (Reynolds and Keveme, Sexually inexperienced Sprague-Dawley male golden hamsters (Meso- 1979; Sanchez-Criado, 1982), the timing of puberty (Lomas et cricetus auratus), bred in the laboratory, were maintained on a reversed al., 1982; Sanchez-Criado, 1982), and in some circumstances, 14 L/IO D light cycle. Six groups of animals were used to study the ovulation and pregnancy (Lloyd Thomas et al., 1982; Beltra- pattern of activation of various brain regions by vomeronasal input. These were intact mated (Ism, n = 8), intact HVF exposed (Is HVF, n mino et al., 1983). Disruption of VN input to the CNS inhibits = 4), intact unstimulated (Ius, n = 7), and equivalent groups with vom- some or all of these responses in various species (Meredith, eronasal organs removed (VNX); VNX stimulated (Vs, n = 7) bilateral 1983; Wysocki and Meredith, 1987). VNX, HVF stimulated (Vs HVF, n = 3) unilateral VNX, HVF stim- We present here results from experiments designed to identify ulated (Vs uni, n = 3) and VNX unstimulated (Vus, n = 10). Most vomeronasal and other contributions to central brain regions VNX animals did not mate, but two additional VNX animals did mate and are presented as a separate group: VNX animals that mated (Vsm). activated during mating behavior or exposure to female che- All VNX animals had their vomeronasal organs (VNOs) removed at mosignals in male hamsters. We used c-fos expression (Morgan 17 d when it was easier to remove all of the organ. The procedure has et al., 1987; Sagar et al., 1988) as a marker of neuronal acti- previously been shown to give reliable deficits similar to those resulting vation, identifying activated neurons in the brain and olfactory from adult removal (Meredith, 1986; Femandez and Meredith, 199 1). Littermates were assigned randomly to VNX and intact surgical groups. bulbs by Fos protein immunocytochemistry. Fos expression was VNOs were excised through the palate under sterile conditions while analyzed following mating behavior, exposure to female hamster the animals were under pentobarbital anesthesia (80 mg/kg, i.p.). The vaginal fluid (HVF), and in control conditions in both intact palate was then closed with cyanoacrylate tissue adhesive and left to animals and in animals whose vomeronasal organs had been heal. All experimental animals were tested behaviorally at 2-3 months removed (VNX). Hamsters are very dependent on chemosen- of age. For behavioral testing, the sexually inexperienced male hamsters, both intact and VNX, were placed in a clean plastic box 42 cm x 20 sory input for mating behavior, but other inputs may also affect cm x 20 cm with fresh bedding and left for 1 min to get accustomed c-fos expression patterns during mating. Fos activation could to their surroundings. They were then presented successively with two be attributable to chemosensory inputs, other sensory inputs, or three naturally cycling, behaviorally receptive females and allowed or mating-related inputs including the motor and integrative to mate for 45 min. The female was changed once or twice for maximal stimulation. After 45 min of mating, the male was left alone for another aspects of behavioral performance. Female HVF contains pher- 45 min before being killed with an overdose of sodium pentobarbital omonal stimuli known to act through the vomeronasal system and perfused for c-fos immunocvtochemistrv. For stimulation with HVF (Clancy et al., 1984). It has both attractant and aphrodisiac a similar procedure was used, except that male hamsters were presented (pheromonal) properties that can elicit mating behavior in male with HVF, approximately 0.2 ml diluted 1: 10 with distilled water placed hamsters (Johnston, 1977), but alone it provides no opportunity in a glass well slide and replenished four or five times, for up to 45 min, after which the animal was left alone for 45 min before being killed and for mating performance. Animals exposed to HVF have the perfused for c-fos immunocytochemistry. Controls, that is, unstimu- stimulus largely restricted to the VN and main olfactory systems. lated, intact, and VNX animals, were placed in a clean box with fresh Activity related to mating performance and female cues other bedding for 90 min and, as for the stimulated animals, the cage lid was than HVF can be eliminated in this way. Analysis of Fos ex- opened at least twice providing some mildly arousing stimulus during this period.
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