Characterization of oxytocin and vasopressin receptors in the Southern giant pouched rat and comparison to other rodents

Abstract

Vasopressin and oxytocin are well known and evolutionarily ancient modulators of social behavior. The distribution and relative densities of vasopressin and oxytocin receptors are known to modulate the sensitivity to these signaling molecules. Comparative work is needed to determine which neural networks have been conserved and modified over evolutionary time, and which social behaviors are commonly modulated by nonapeptide signaling. To this end, we used receptor autoradiography to determine the distribution of vasopressin 1a and oxytocin receptors in the Southern giant pouched rat (Cricetomys ansorgei) brain, and to assess the relative densities of these receptors in specific brain regions. We then compared the relative receptor pattern to 23 other species of rodents using a multivariate ANOVA. Pouched rat receptor patterns were strikingly similar to hamsters and voles overall, despite the variation in social organization among species. Uniquely, the pouched rat had dense vasopressin 1a receptor binding in the caudate-putamen (i.e., striatum), an area that might impact affiliative behavior in this species. In contrast, the pouched rat had relatively little oxytocin receptor binding in much of the anterior forebrain. Notably, however, oxytocin receptor binding demonstrated extremely dense binding in the bed nucleus of the stria terminalis, which is associated with the modulation of several social behaviors and a central hub of the social decision-making network. Examination of the nonapeptide system has the potential to reveal insights into species-specific behaviors and general themes in the modulation of social behavior.

Keywords: autoradiography; nonapeptide; social behavior; social organization; striatum.

Figure 1

OTR in the pouched rat brain. Images on the left of each pair are Nissl stain, with associated autoradiograms on the right showing OTR density. OB: Olfactory bulb, AON: Accessory olfactory nucleus, PFC: Prefrontal Cortex, MCtx: Motor Cortex, CP: Caudate putamen, LS: Lateral septum, NAc: Nucleus accumbens, VPall: Ventral pallidum, icj: Islands of Calleja, BST: Bed nucleus of the stria terminalis, mPOA: Medial preoptic area, OlfTub: Olfactory tubercle, Pir: Piriform area, PVT: paraventricular thalamus, ZIR: Zona incerta, PVN: Paraventricular nucleus of the hypothalamus, EP: Endopiriform area, BLA: Basolateral amydgala, MeA: Medial amygdala, CeA: Central amygdala, VMH: Ventromedial hypothalamus, CA3: CA3 region of the hippocampus, PAG: Periaqueductal gray, PH: Posterior hypothalamus, SuM: Supramammilary nucleus, CA1: CA1 region of the hippocampus, SC: Superior colliculus. Not shown: VTA: Ventral tegmental area.

Figure 2

V1aR in the pouched rat brain. Images on the left of each pair are Nissl stain, with associated autoradiograms on the right showing OTR density. OB: Olfactory bulb, AON: Accessory olfactory nucleus, PFC: Prefrontal Cortex, ILA: Infralimbic region of the prefrontal cortex, MCtx: Motor Cortex, CP: Caudate putamen, LS: Lateral septum, NAc: Nucleus accumbens, VPall: Ventral pallidum, icj: Islands of Calleja, BST: Bed nucleus of the stria terminalis, mPOA: Medial preoptic area, OlfTub: Olfactory tubercle, Pir: Piriform area, PVT: paraventricular thalamus, ZIR: Zona incerta, EP: Endopiriform area, BLA: Basolateral amydgala, MeA: Medial amygdala, CeA: Central amygdala, LH: Lateral hypothalamys, VMH: Ventromedial hypothalamus, CA3: CA3 region of the hippocampus, PAG: Periaqueductal gray, PH: Posterior hypothalamus, SuM: Supramammilary nucleus, CA1: CA1 region of the hippocampus, SC: Superior colliculus, VTA: ventral tegmental area.

Figure 3

PCA biplot of OTR binding patterns with the number of regions included maximized. Species included in this analysis are 1) Acomys cahirinus, 2) Cavia porcellus, 3) Cricetomys ansorgei, 4a) Ctenomys sociabilis, 4b) Ctenomys haigi, 5) Heterocephalus glaber, 6) Meriones shawi, 7a) Microtus ochrogaster, 7b) Microtus kikuchii, 7c) Microtus pennsylvanicus, 8) Mus musculus, 9) Octodon degu, 10a) Otomys sloggett, 10b) Otomys auratus, 11) Rattus norvegicus, 15a) Scotinomys xerampelinus, 12b) Scotinomys teguina, 13) Urocitellus richardsonii.

Figure 4

PCA biplot of OTR binding patterns with the number of species included maximized. Species included in this analysis are 1) Acomys cahirinus, 2) Cavia porcellus, 3) Cricetomys ansorgei, 4a) Ctenomys sociabilis, 4b) Ctenomys haigi, 5) Georychus capensis, 6) Heterocephalus glaber, 7a) Meriones unguiculatus, 7b) Meriones shawi, 8) Mesocricetus auratus, 9a) Microtus ochrogaster, 9b) Microtus montanus, 9c) Microtus kikuchii, 9d) Microtus pennsylvanicus, 10) Mus musculus, 11) Octodon degu, 12a) Otomys sloggett, 12b) Otomys auratus, 13a) Peromyscus maniculatus, 13b) Peromyscus californicus, 14) Rattus norvegicus, 15a) Scotinomys xerampelinus, 15b) Scotinomys teguina, 16) Urocitellus richardsonii.

Figure 5

PCA biplot of V1aR binding patterns with the number of species included maximized. Species included in this analysis are 1) Acomys cahirinus, 2) Cricetomys ansorgei, 3a) Ctenomys sociabilis, 3b) Ctenomys haigi, 4) Jaculus orientalis, 5a) Meriones shawi, 5bc) Meriones unguiculatus, 6) Mesocricetus auratus, 7a) Microtus ochrogaster, 7b) Microtus montanus, 7c) Microtus kikuchii, 7d) Microtus pennsylvanicus, 8) Mus musculus, 9a) Peromyscus maniculatus, 9b) Peromyscus californicus, 10) Phodupus sungorus, 11) Rattus norvegicus, 12a) Scotinomys xerampelinus (note, this point fell directly below 1, A. cahirinus), 12b) Scotinomys teguina, 13) Urocitellus richardsonii.

Figure 6

PCA biplot of V1aR binding patterns with the number of regions included maximized. Species included in this analysis are 1) Cricetomys ansorgei, 2) Jaculus orientalis, 3) Meriones unguiculatus, 4a) Microtus ochrogaster, 4b) Microtus montanus, 5) Mus musculus, 6a) Peromyscus maniculatus, 6b) Peromyscus californicus, 7) Phodupus sungorus, 8) Rattus norvegicus, 9a) Scotinomys xerampelinus, 9b) Scotinomys teguina, 10) Urocitellus richardsonii.