title: Characteristic neurobiological patterns differentiate paternal responsiveness in two Peromyscus species.
abstract: Rodent paternal models provide unique opportunities to investigate the emergence of affiliative social behavior in mammals. Using biparental and uniparental Peromyscus species (californicus and maniculatus, respectively) we assessed paternal responsiveness by exposing males to biological offspring, unrelated conspecific pups, or familiar brothers following a 24-hour separation. The putative paternal circuit we investigated included brain areas involved in fear/anxiety [cingulate cortex (Cg), medial amygdala (MeA), paraventricular nucleus of the hypothalamus (PVN), and lateral septum (LS)], parental motivation [medial preoptic area (MPOA)], learning/behavioral plasticity (hippocampus), olfaction [pyriform cortex (PC)], and social rewards (nucleus accumbens). Paternal experience in californicus males reduced fos immunoreactivity (ir) in several fear/anxiety areas; additionally, all californicus groups exhibited decreased fos-ir in the PC. Enhanced arginine vasopressin (AVP) and oxytocin (OT)-ir cell bodies and fibers, as well as increased neuronal restructuring in the hippocampus, were also observed in californicus mice. Multidimensional scaling analyses revealed distinct brain activation profiles differentiating californicus biological fathers, pup-exposed virgins, and pup-naïve virgins. Specifically, associations among MPOA fos, CA1 fos, dentate gyrus GFAP, CA2 nestin-, and PVN OT-ir characterized biological fathers; LS fos-, Cg fos-, and AVP-ir characterized pup-exposed virgins, and PC-, PVN-, and MeA fos-ir characterized pup-naïve virgins. Thus, whereas fear/anxiety areas characterized pup-naïve males, neurobiological factors involved in more diverse functions such as learning, motivation, and nurturing responses characterized fatherhood in biparental californicus mice. Less distinct paternal-dependent activation patterns were observed in uniparental maniculatus mice. These data suggest that dual neurobiological circuits, leading to the inhibition of social-dependent anxiety as well as the activation of affiliative responses, characterize the transition from nonpaternal to paternal status in californicus mice.
authors.affiliation: Department of Psychology, Randolph-Macon College, Ashland, Va., USA. klambert@rmc.edu
authors.forename: Kelly G
authors.initials: KG
authors.lastname: Lambert
authors.forename: Catherine L
authors.initials: CL
authors.lastname: Franssen
authors.forename: Massimo
authors.initials: M
authors.lastname: Bardi
authors.forename: Joseph E
authors.initials: JE
authors.lastname: Hampton
authors.forename: Leslie
authors.initials: L
authors.lastname: Hainley
authors.forename: Stephanie
authors.initials: S
authors.lastname: Karsner
authors.forename: Eddie B
authors.initials: EB
authors.lastname: Tu
authors.forename: Molly M
authors.initials: MM
authors.lastname: Hyer
authors.forename: Ashly
authors.initials: A
authors.lastname: Crockett
authors.forename: Anya
authors.initials: A
authors.lastname: Baranova
authors.forename: Tajh
authors.initials: T
authors.lastname: Ferguson
authors.forename: Tenaj
authors.initials: T
authors.lastname: Ferguson
authors.forename: Craig H
authors.initials: CH
authors.lastname: Kinsley
mesh_terms: D000679:Amygdala / Q000502:physiology; D000818:Animals; D001522:Behavior, Animal / Q000502:physiology*; D001921:Brain / Q000502:physiology*; D001931:Brain Mapping; D006179:Gyrus Cinguli / Q000502:physiology; D006624:Hippocampus / Q000502:physiology; D007381:Intermediate Filament Proteins / Q000378:metabolism; D008297:Male; D009419:Nerve Tissue Proteins / Q000378:metabolism; D064231:Nestin; D009434:Neural Pathways / Q000502:physiology*; D009473:Neuronal Plasticity / Q000502:physiology; D009714:Nucleus Accumbens / Q000502:physiology; D016761:Oncogene Proteins v-fos / Q000378:metabolism; D010286:Paraventricular Hypothalamic Nucleus / Q000502:physiology; D010332:Paternal Behavior / Q000502:physiology*; D010542:Peromyscus / Q000502:physiology*; D011301:Preoptic Area / Q000502:physiology; D021641:Recognition, Psychology / Q000502:physiology; D012686:Septal Nuclei / Q000502:physiology; D012919:Social Behavior; D013045:Species Specificity
chemical_list: D007381:Intermediate Filament Proteins; D009419:Nerve Tissue Proteins; C577485:Nes protein, mouse; D064231:Nestin; D016761:Oncogene Proteins v-fos