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Oxytocin and Vasopressin Immunoreactive Staining in the Brains of Brandt's Voles (Lasiopodomys Brandtii) and Greater Long-Ta

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Oxytocin and Vasopressin Immunoreactive Staining in the Brains of Brandt's Voles (Lasiopodomys Brandtii) and Greater Long-Ta Neuroscience 169 (2010) 1235–1247 OXYTOCIN AND VASOPRESSIN IMMUNOREACTIVE STAINING IN THE BRAINS OF BRANDT’S VOLES (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 Rodents 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 rodent 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 (Microtus (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 vole 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 animal 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,
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