Neuroscience 169 (2010) 1235–1247

OXYTOCIN AND VASOPRESSIN IMMUNOREACTIVE STAINING IN THE BRAINS OF BRANDT’S (LASIOPODOMYS BRANDTII) AND GREATER LONG-TAILED HAMSTERS (TSCHERSKIA TRITON)

L. XU,a Y. PAN,a K. A. YOUNG,b Z. WANGb neural mechanisms. Using a comparative approach, re- AND Z. ZHANGa* markable differences have been found in several types of aState Key Laboratory of Integrated Management of Pest Insects and social behaviors, and these differences, when grouped in Agriculture, Institute of Zoology, Chinese Academy of together, constitute general life strategies. Species that Sciences, Datun Road, Chaoyang District, Beijing 100101, PR China follow a monogamous life strategy, for example, usually bDepartment of Psychology and Program in Neuroscience, Florida exhibit high levels of social affiliation among individuals, State University, Tallahassee, FL 32306, USA biparental care for their offspring, and selective aggression towards unfamiliar conspecifics (Kleiman, 1977; Dews- Abstract—Immunoreactive (ir) staining of the neuropeptides bury, 1987). In contrast, non-monogamous species tend to oxytocin (OT) and vasopressin (AVP) was performed in the be solitary, less affiliative, and more aggressive. Such brains of Brandt’s voles (Lasiopodomys brandtii) and greater species differences in behavior may reflect evolutionary long-tailed hamsters (Tscherskia triton)—two species that differ pressure and/or a specific adaptation to the environment. remarkably in social behaviors. Social Brandt’s voles had In addition, such differences may indicate potential under- higher densities of OT-ir cells in the medial preoptic area (MPOA) and medial amygdala (MeA) as well as higher densities lying species differences in the central nervous system. of AVP-ir cells in the lateral hypothalamus (LH) compared to Several elegant models have been developed solitary greater long-tailed hamsters. In contrast, the hamsters to examine species-specific behaviors and underlying neu- had higher densities of OT-ir cells in the anterior hypothalamus ral patterns. By comparing monogamous prairie ( (AH) and LH and higher densities of AVP-ir cells in the MPOA ochrogaster) and pine (M. pinetorum) voles with promis- than the voles. OT-ir and AVP-ir fibers were also found in many cuous montane (M. montanus) and meadow (M. pennsyl- forebrain areas with subtle species differences. Given the roles vanicus) voles, differences have been found in several of OT and AVP in the regulation of social behaviors in other rodent species, our data support the hypothesis that species- patterns of social behaviors, including pair bonding, paren- specific patterns of central OT and AVP pathways may underlie tal care, and selective aggression (Getz et al., 1981; species differences in social behaviors. However, despite a McGuire and Novak, 1984, 1986; Oliveras and Novak, higher density of OT-ir cells in the paraventricular nucleus of 1986; Shapiro and Dewsbury, 1990), and such differences the hypothalamus (PVN) in females than in males in both spe- in behaviors have been correlated with species differences cies, no other sex differences were found in OT-ir or AVP-ir stain- in central neurotransmitter systems including oxytocin ing. These data failed to support our prediction that a sexually (OT), vasopressin (AVP), and dopamine (DA) (Insel and dimorphic pattern of neuropeptide staining in the brain is more apparent in Brandt’s voles than in greater long-tailed hamsters. Shapiro, 1992; Insel et al., 1994; Wang et al., 1997; Ara- © 2010 IBRO. Published by Elsevier Ltd. All rights reserved. gona et al., 2006; Young et al., 2008). Further, pharmaco- logical and molecular manipulations in monogamous and Key words: medial preoptic area, anterior hypothalamus, me- promiscuous species have shown that OT, AVP, and dial amygdala, solitary, social behavior. DA play important roles in regulating social behaviors as- sociated with a monogamous life strategy (Winslow et al., Species comparisons are a powerful tool used in experi- 1993; Williams et al., 1994; Lim et al., 2004; Aragona et al., mental biology to study behavior and its underlying 2006). A similar comparative approach has also been ap- plied to the study of social behavior and its underlying ϩ ϩ *Corresponding author. Tel: 86-10-62554027; fax: 86-10-62565689. neural mechanisms in mice. Monogamous California mice E-mail address: [email protected] (Z. Zhang). Abbreviations: AH, anterior hypothalamus, (anterior part); AHP, ante- (Peromyscus californicus) are highly social and display rior hypothalamus, posterior; BST, bed nucleus of the stria terminalis; biparental behavior whereas promiscuous male white- BSTL, bed nucleus of the stria terminalis, lateral; BSTMA, bed nucleus footed mice (P. leucopus) are primarily solitary during the of the stria terminalis, anterior, medial; BSTMPL, bed nucleus of the stria terminalis, posterior, lateral, medial; BSTV, bed nucleus of the breeding season and exhibit less paternal behavior (Mad- stria terminalis, ventral; LH, lateral hypothalamic area; LS, lateral ison et al., 1984; Bester-Meredith et al., 1999). It has been septum; MeA, medial amygdaloid nucleus; MnPO, median preoptic shown that these species differences in social behaviors nucleus; MPOA, medial preoptic area; MPOAa, medial preoptic area, are correlated with differences in the extra-hypothalamic anterior; MPOAi, medial preoptic area, intermediate; MPOAp, medial preoptic area, posterior; opt, optic tract; Pe, pariventricular hypotha- AVP pathway, particularly the AVP pathway in the bed lamic nucleus; PVN, paraventricular nucleus of the hypothalamus; Rt, nucleus of the stria terminalis (BST) and the medial nu- reticular thalamic nucleus; SCN, suprachiasmatic nucleus; SI, sub- cleus of the amygdala (MeA) (Bester-Meredith et al., 1999; stantia innominata; SM, nucleus of stria medullaris; SON, supraoptic nucleus; SOX, supraoptic decussation; VMH, ventromedial hypothal- Bester-Meredith and Marler, 2001, 2003). Furthermore, in amus; 3V, third ventricle. a recent study in two related South American rodent spe- 0306-4522/10 $ - see front matter © 2010 IBRO. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.neuroscience.2010.05.064

1235 1236 L. Xu et al. / Neuroscience 169 (2010) 1235–1247 cies, the social colonial tuco-tuco (Cetnomys sociabilis) and (Yang et al., 1996; Zhang et al., 1998b). They reach sexual solitary Patagonian tuco-tuco (Ctenomys haigi), species maturity around 1.5 months of age, and their life span is differences were found in OT and AVP receptor distribu- about 1 year in the wild and 3–4 years in laboratory con- tions in the brain, implicating OT and AVP in the behavioral ditions (Zhang et al., 1998b). These hamsters live in soli- differences noted between these species (Beery et al., tude throughout the year and participate in limited social 2008). Interestingly, in a study comparing several monog- affiliation with conspecifics, except during breeding sea- amous avian species (family Estrildidae), the receptor den- sons (Zhang et al., 1999, 2001b). Males and females do sities for vasotocin (an OT/AVP analog found in non-mam- not differ in their body sizes and both display similar levels malian vertebrates) in the brain were related positively to of flank marking behavior and aggression (Zhang et al., sociality (Goodson et al., 2006). 2001a; Wang et al., 2006). Although differences in social OT and AVP are both nine amino-acid neuropeptides that behaviors have been shown between the two species (Yin are primarily synthesized in the paraventricular (PVN) and and Fang, 1998; Zhang et al., 1999, 2001b; Chen and Shi, supraoptic (SON) nuclei of the hypothalamus, transported 2003), we know little about the underlying neurochemical into the posterior pituitary gland, and then released into the systems. As central OT and AVP systems have been blood stream to mediate physiological functions in a variety of implicated in species-specific patterns of social behaviors species (Brownstein et al., 1980). OT has been shown to play in other rodent species, we hypothesized that Brandt’s an important role in uterine contraction and milk letdown voles and greater long-tailed hamsters differ in their OT (Caldeyrobarcia and Poseiro, 1960; Young et al., 1996), and AVP systems which, in turn, may regulate their differ- whereas AVP regulates water re-absorption and blood pres- ences in social behaviors. In the current study, as the first sure (Edmunds and West, 1962; Nielsen et al., 1995). How- step to test this hypothesis, we compared OT and AVP ever, OT or AVP synthesizing cells are also found in other immunoreactive (ir) staining in the brains of these two brain areas, such as the anterior hypothalamus (AH), medial species. We predicted that the two species may differ in preoptic area (MPOA), BST and MeA (DeVries et al., 1985; the distribution pattern and regional quantity of OT and/or Young and Gainer, 2003; Rosen et al., 2008). These cells AVP staining, correlating with their differences in social project centrally into forebrain areas in which OT and AVP behaviors. In addition, we hypothesized that sexually di- are released to regulate cognitive and behavioral functions, morphic patterns in OT and/or AVP staining would be more including parental behavior, pair bonding, social recognition, apparent in the Brandt’s voles than in the greater long- learning and memory (Dantzer et al., 1988; Ferguson et al., tailed hamsters, as the former species demonstrates more 2002; Caldwell et al., 2008). In addition, central AVP has sexually dimorphic behavioral patterns than the latter (Yin been implicated in flank marking (a stereotypical scent mark- and Fang, 1998; Zhang et al., 2001a; Chen and Shi, 2003). ing behavior commonly displayed by hamsters) and aggres- sion in males (Ferris et al., 1984, 1988; Everts et al., 1997). EXPERIMENTAL PROCEDURES Interestingly, comparative studies have illustrated species differences in central OT and AVP pathways and their recep- Subjects tors and these differences have been implicated in species- Subjects were adult (3 months of age) male and female Brandt’s specific life strategies and social behaviors (Insel and Sha- voles (Lasiopodomys brandtii) and greater long-tailed hamsters piro, 1992; Insel et al., 1994; Bester-Meredith et al., 1999). (Tscherskia triton). Subjects were offspring of laboratory breeding Furthermore, sex differences have also been found in central colonies started with field captured and maintained in the Institute of Zoology at the Chinese Academy of Sciences in Bei- OT and AVP systems, implicating the role of those systems in jing, China. All subjects were maintained in plastic cages (25ϫ regulating sex-specific cognitive and behavioral functions (De 14ϫ14 cm3 for Brandt’s vole; 27ϫ16ϫ13 cm3 for greater long- Vries and Panzica, 2006; Carter, 2007). tailed hamster) that contained wood shavings. Food and water In the present study, we compared two local rodent were provided ad libitum. Brandt’s voles were housed in same-sex species that belong to the family. Brandt’s voles groups, consisting of two to three individuals each, under a (Lasiopodomys brandtii) inhabit typical steppes in Inner 16L:8D photoperiod (lights on 0500) while greater long-tailed hamsters were housed singly under a reversed 16L:8D photoperiod Mongolia of China, Mongolia, and the region of Beigaer in (lights on 1700). These housing conditions were chosen based upon Russia (Shi, 1988; Liu et al., 1994). They usually become the natural behaviors displayed by each species. Room temperature sexually mature around 1.5 months of age, and their life was maintained at 20Ϯ2 °C. All experimental procedures complied span is about 1 year in the wild and 2.5 years in the with the guidelines for animal use and care as stipulated by the laboratory (Zhang et al., 1998a). Brandt’s voles are social Institute of Zoology at the Chinese Academy of Sciences. animals that live in large family groups and display exten- sive social interactions among individuals (Yin and Fang, Tissue preparation 1998; Wan et al., 1999; Chen and Shi, 2003). Sex differ- Eight males and eight females of each species were deeply anes- ences in this species are found in both morphology and thetized with sodium pentobarbital (3 mg/100 g body weight, behavior, with males being larger and displaying higher Sigma-Aldrich, St. Louis, MO, USA) and perfused through the levels of territorial defense than females (Hou and Yin, ascending aorta with 0.1 M phosphate buffered solution (PBS, pHϭ7.2) followed by 4% paraformaldehyde in PBS. Brains were 1996; Yin and Fang, 1998; Chen and Shi, 2003). In con- quickly removed, post-fixed in 4% paraformaldehyde for 12 h, and trast, greater long-tailed hamsters (Tscherskia triton) are then stored in 30% sucrose in PBS. Coronal brain sections of distributed primarily in the farmland and wilderness of 40-␮m thickness were cut on a cryostat. Two alternate sets of northern China, the region of Siberia in Russia, and Korea brain sections at 240-␮m intervals were processed for OT and Download English Version: https://daneshyari.com/en/article/6277020

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