Fatherhood contributes to increased hippocampal spine density and anxiety regulation in California mice

Glasper

2017

PLoS ONE

Self Cite

Individuals within monogamous species form bonds that may buffer against the negative effects of stress on physiology and behavior. In some species, involuntary termination of the mother-offspring bond results in increased symptoms of negative affect in the mother, suggesting that the parent-offspring bond may be equally as important as the pair bond. To our knowledge, the extent to which affect in paternal rodents is altered by involuntary termination of the father-offspring bond is currently unknown. Here, we investigated to what extent separation and paternal experience alters passive stress-coping behaviors and dendritic morphology in hippocampal subfields of California mice (Peromyscus californicus). Irrespective of paternal experience, separated mice displayed shorter latencies to the first bout of immobility, longer durations of immobility, and more bouts of immobility than control (non-separated) mice. This effect of separation was exacerbated by paternal experience in some measures of behavioral despair—separation from offspring further decreased the latency to immobility and increased bouts of immobility. In the dentate gyrus, separation reduced dendritic spine density regardless of paternal experience. Increased spine density was observed on CA1 basal, but not apical, dendrites following paternal experience. Regardless of offspring presence, fatherhood was associated with reduced apical dendritic spine density in area CA3 of the hippocampus. Separation enhanced complexity of both basal and apical dendrites in CA1, while fatherhood reduced dendritic complexity in this region. Our data suggest that forced dissolution of the pair bond induces passive stress-coping behaviors and contributes to region-specific alterations in hippocampal structure in California mouse males.

Section: Discussionsupporting

confidence: 45%

Separation increases passive stress-coping behaviors during forced swim and alters hippocampal dendritic morphology in California mice

Glasper

2017

PLoS ONE

Self Cite

“…More recent findings suggest that offspring contact‐induced reductions in anxiety‐like behavior may also be the case in fathers. We have recently observed a decrease in anxiety‐like behavior at PND 19 in California mouse fathers (Glasper et al ., ). Given that the anxiolytic profile, in our present study and prior work, does not develop until ~ 2 weeks post‐birth, it is possible that increased pup retrieval observed at this time point in the California mouse may be directly contributing to our observed effects on emotional regulation.…”

Section: Discussionmentioning

confidence: 97%

“…The California mouse ( Peromyscus californicus ) exhibits extensive paternal care (Gubernick & Alberts, ) that has been well‐characterized (Bester‐Meredith et al ., ), providing a model with which to explore fatherhood‐induced changes in emotional regulation. We recently observed a decrease in PPA‐like behavior on postnatal day (PND) 19 in California mouse males (Glasper et al ., ), a time of reported peak retrievals by fathers of straying pups (Bester‐Meredith et al ., ). However, the extent to which altered anxiety‐like behavior is specific to this time during the postpartum period, and to what extent anxiety‐like behavior is associated with structural changes within the brain, remains unknown.…”

Section: Introductionmentioning

confidence: 99%

Neurogenesis and anxiety‐like behavior in male California mice during the mate's postpartum period

Hunter

Katakam

et al. 2016

Eur J of Neuroscience

Our understanding of postpartum anxiety (PPA) in fathers is limited, despite the negative consequences of anxiety on the father and child. Offspring contact reduces PPA in mothers; however, parallel investigations in fathers has gone unaddressed. Adult neurogenesis in the dentate gyrus (DG) contributes to anxiety regulation and is altered during the postpartum period, yet the effects of fatherhood on the production, or survival, of newborn cells in the DG, and the role of adult neurogenesis in PPA regulation, have not been examined. Using the biparental California mouse (Peromyscus californicus), we examined the relationships among postnatal day, anxiety-like behavior and adult neurogenesis in fathers. We hypothesized that attenuated anxiety-like behavior and enhanced adult neurogenesis would be observed when father-offspring contact was increased. We observed a reduction in anxiety-like behavior on the elevated plus-maze, but only at PND 16, a time of peak pup retrieval. Fatherhood reduced 1-week survival of newborn cells; however, surviving cells were maintained until 2 weeks postpartum. In contrast, non-fathers experienced a significant reduction in the survival of newborn cells between 1 and 2 weeks postpartum. Fatherhood also increased the numbers of newborn cells that expressed a neuronal phenotype. Collectively, these findings suggest that offspring interaction contributes to reductions in anxiety-like behavior and the maintenance of newborn neurons in the DG of fathers. These data contribute to our knowledge of the postpartum affective state in fathers, findings that may contribute to improved health of both the father and offspring.

“…Recordings were taken from a top-down view at a rate of 30 frames per second. Latency to enter the arms, duration of time spent in the arms, and number of arm entries were assessed as previously described (Glasper et al, 2015 ; Hyer et al, 2016 ). Duration of time spent in the open arms was calculated as total time spent in the open arms divided by the total time spent in both the open and closed arms, excluding the center, multiplied by 100 and presented as a percentage.…”

Section: Methodsmentioning

confidence: 99%

Enduring Effects of Paternal Deprivation in California Mice (Peromyscus californicus): Behavioral Dysfunction and Sex-Dependent Alterations in Hippocampal New Cell Survival

Glasper

Front. Behav. Neurosci.

Hunter

2018

Self Cite

Early-life experiences with caregivers can significantly affect offspring development in human and non-human animals. While much of our knowledge of parent-offspring relationships stem from mother-offspring interactions, increasing evidence suggests interactions with the father are equally as important and can prevent social, behavioral, and neurological impairments that may appear early in life and have enduring consequences in adulthood. In the present study, we utilized the monogamous and biparental California mouse (Peromyscus californicus). California mouse fathers provide extensive offspring care and are essential for offspring survival. Non-sibling virgin male and female mice were randomly assigned to one of two experimental groups following the birth of their first litter: (1) biparental care: mate pairs remained with their offspring until weaning; or (2) paternal deprivation (PD): paternal males were permanently removed from their home cage on postnatal day (PND) 1. We assessed neonatal mortality rates, body weight, survival of adult born cells in the dentate gyrus of the hippocampus, and anxiety-like and passive stress-coping behaviors in male and female young adult offspring. While all biparentally-reared mice survived to weaning, PD resulted in a ~35% reduction in survival of offspring. Despite this reduction in survival to weaning, biparentally-reared and PD mice did not differ in body weight at weaning or into young adulthood. A sex-dependent effect of PD was observed on new cell survival in the dentate gyrus of the hippocampus, such that PD reduced cell survival in female, but not male, mice. While PD did not alter classic measures of anxiety-like behavior during the elevated plus maze task, exploratory behavior was reduced in PD mice. This observation was irrespective of sex. Additionally, PD increased some passive stress-coping behaviors (i.e., percent time spent immobile) during the forced swim task—an effect that was also not sex-dependent. Together, these findings demonstrate that, in a species where paternal care is not only important for offspring survival, PD can also contribute to altered structural and functional neuroplasticity of the hippocampus. The mechanisms contributing to the observed sex-dependent alterations in new cell survival in the dentate gyrus should be further investigated.